Article

Place cells recorded in the parasubiculum of freely moving rats

January 1995
Hippocampus 5(6):569-83

January 1995
5(6):569-83

DOI:10.1002/hipo.450050608

Source
PubMed

Authors:

Jeffrey S Taube

Dartmouth College

Previous studies have identified neurons in the hippocampus, subiculum, and entorhinal cortex which discharge as a function of the animal's location in the environment. In contrast, neurons in the postsubiculum and anterior thalamic nucleus discharge as a function of the animal's head direction in the horizontal plane, independent of its behavior and location in the environment. Because the parasubiculum (PaS) has extensive connections, either directly or indirectly, with these structures, it is centrally located to influence the neuronal activity in these areas. This study was therefore designed to determine the types of behavioral and spatial correlates in neurons from the PaS. Single unit recordings were conducted in the PaS of freely moving rats trained to retrieve food pellets thrown randomly into a cylindrical apparatus. A total of 10.3% of the cells were classified as place cells because they discharged in relation to the animal's location in the cylinder. A large percentage of cells (41.4%) were classified as theta cells. The remaining cells had nondiscernable behavioral correlates.

Contribution of Ih to the relative facilitation of synaptic responses induced by carbachol in the entorhinal cortex during repetitive stimulation of the parasubiculum

Article

Aug 2014

Neurons in the superficial layers of the entorhinal cortex provide the hippocampus with the majority of its cortical sensory input, and also receive the major output projection from the parasubiculum. This puts the parasubiculum in a position to modulate the activity of entorhinal neurons that project to the hippocampus. These brain areas receive cholinergic projections that are active during periods of theta and gamma-frequency EEG activity. The purpose of this study was to investigate how cholinergic receptor activation affects the strength of repetitive synaptic responses at these frequencies in the parasubiculo-entorhinal pathway and the cellular mechanisms involved. Whole-cell patch clamp recordings of layer II medial entorhinal neurons were conducted using an acute slice preparation, and responses to 5-pulse trains of stimulation at theta and gamma-frequency delivered to the parasubiculum were recorded. The cholinergic agonist carbachol suppressed the amplitude of single synaptic responses, but also produced a relative facilitation of synaptic responses evoked during stimulation trains. The NMDA glutamate receptor blocker APV did not significantly reduce the relative facilitation effect. However, the Ih channel blocker ZD7288 mimicked the relative facilitation induced by carbachol, suggesting that carbachol-induced inhibition of Ih could produce the effect by increasing dendritic input resistance. Inward-rectifying and leak K(+) currents are known to interact with Ih to affect synaptic excitability. Application of the K(+) channel antagonist Ba(2+) depolarized neurons and enhanced temporal summation, but did not block further facilitation of train-evoked responses by ZD7288. The Ih-dependent facilitation of synaptic responses can therefore occur during reductions in IKir associated with dendritic depolarization. Thus, in addition to cholinergic reductions in transmitter release that are known to facilitate train-evoked responses, these findings emphasize the role of inhibition of Ih in the integration of synaptic inputs within the entorhinal cortex during cholinergically-induced oscillatory states, likely due to enhanced summation of EPSPs induced by increases in dendritic input resistance.

Cholinergic receptor activation induces a relative facilitation of synaptic responses in the entorhinal cortex during theta- and gamma-frequency stimulation of parasubicular inputs

Article

Nov 2012

The parasubiculum sends its single major output to layer II of the entorhinal cortex, and it may therefore interact with inputs to the entorhinal cortex from other cortical areas, and help to shape the activity of layer II entorhinal cells that project to the hippocampal formation. Cholinergic inputs are thought to contribute to the generation of theta- and gamma-frequency activities in the parasubiculum and entorhinal cortex, and the present study assessed how cholinergic receptor activation affects synaptic responses of the entorhinal cortex to theta- and gamma-frequency stimulation. Depth profiles of field excitatory postsynaptic potentials (fEPSPs) in acute brain slices showed a short-latency negative fEPSP in layer II, consistent with the activation of excitatory synaptic inputs to layer II. Application of the cholinergic agonist carbachol (CCh) suppressed synaptic responses and enhanced paired-pulse facilitation. CCh also resulted in a marked relative facilitation of synaptic responses evoked during short 5-pulse trains of stimulation at both theta- and gamma-frequencies. Application of the M1 antagonist pirenzepine, but not the M2 antagonist methoctramine, blocked the facilitation of responses. Inhibition of the M-current or block of GABAB receptors had no effect, but the facilitation effect was partially blocked by the N-methyl-d-aspartate (NMDA) antagonist APV, indicating that NMDA receptors play a role. Application of ZD7288, a selective inhibitor of the hyperpolarization-activated cationic current Ih, almost completely blocked the relative facilitation of responses, and the less potent Ih-blocker Cs+ also resulted in a partial block. The relative facilitation of synaptic responses induced by CCh is therefore likely mediated by multiple mechanisms including the cholinergic suppression of transmitter release that enhances transmitter availability during repetitive stimulation, NMDA receptor-mediated effects on pre- or postsynaptic function, and cholinergic modulation of the current Ih. These mechanisms likely contribute to the maintenance of effective synaptic communication within parasubicular inputs to the entorhinal cortex during cholinergically induced rhythmic states.

Excitotoxic Lesions of the Pre- and Parasubiculum Disrupt Object Recognition and Spatial Memory Processes

Article

Full-text available

Feb 2001

Rats with bilateral ibotenic acid lesions centered on the pre- and parasubiculum and control rats were tested in a series of spatial memory and object recognition memory tasks. Lesioned rats were severely impaired relative to controls in both the reference and working memory versions of the water maze task and displayed a delay-dependent deficit in a delayed nonmatch to place procedure conducted in the T-maze. Lesioned rats also displayed reduced exploration in a novel environment, and performance was altered in an object recognition procedure as compared with the control group. These findings indicate that the pre- and parasubiculum plays an important role in the processing of both object recognition and spatial memory.

Place field plasticity and directionality in a spatial memory task

Thesis

Jan 1996

Patrick Dov Martin

In order to determine whether hippocampal units display firing which is modulated by the demands of a spatial memory task rats were trained in an enclosed "cue controlled environment" (CCE) consisting of four platforms and six spatial cues that identified one of the four platforms as the goal. Rats learned to select the goal platform at the end of the trial even when the cues defined the goal platform were removed mid-way through the trial. In a previous study (O'Keefe and Speakman, 1987a) place fields were shown to be controlled by the spatial cues such that rotation of the cues caused concomitant rotation of the fields. They also found that the place fields continued to fire after removal of the cues. Thus although the place fields were controlled by the six spatial cues they were not dependent on them. In the present study we confirm the above findings and report two new responses. Some hippocampal place units were observed to increase or initiate place specific firing after cue removal. Others decreased or ceased place specific firing after cue removal. Thus place field location and place field intensity appears to be governed by the presence or absence of the six spatial cues. Previous work has shown that place fields show directionality when a rat traverses an open field in a restricted and stereotypical manner (McNaughton et al, 1983a; Marcus et al, 1995). Rats trained on the CCE spatial memory task were shaped to run in a raster pattern to insure uniform platform coverage. The place fields recorded in this situation were found to display directionality oriented with respect to the six spatial cues. Moreover the directionality of place fields was found to persist after the six spatial cues were removed. Thus place field directionality appears to be initially configured by the six spatial cues but is subsequently independent of them. O'Keefe and Speakman (1987a) examined error trials in which the rat failed to choose the goal platform. They found that the place field firing displayed by the hippocampus before the rat chose a platform could be used to predict the rat's choice. In the present study the hippocampal error trial firing could be use to predict the choice the rat made in some instances as per O'Keefe and Speakman (1987a). However in the majority of instances the hippocampal error trial firing was completely unrelated to that seen in previously recorded correct trials and in one instance the hippocampal error trial firing predicted that the rat would choose correctly.

Electrophysiological and Molecular Characterization of the Parasubiculum

Article

Full-text available

Sep 2019

The parahippocampal region is thought to be critical for memory and spatial navigation. Within this region lies the parasubiculum, a small structure that exhibits strong theta modulation, contains functionally specialised cells and projects to layer II of the medial entorhinal cortex (MEC). Thus, it is uniquely positioned to influence firing of spatially modulated cells in the MEC and play a key role in the internal representation of the external environment. However, the basic neuronal composition of the parasubiculum remains largely unknown, and its border with the MEC is often ambiguous. We combine electrophysiology and immunohistochemistry in adult mice (both sexes) to define first, the boundaries of the parasubiculum, and second, the major cell types found in this region. We find distinct differences in the colabelling of molecular markers between the parasubiculum and the MEC, allowing us to clearly separate the two structures. Moreover, we find distinct distribution patterns of different molecular markers within the PaS, across both superficial-deep and dorsal-ventral axes. Using unsupervised cluster analysis, we find that neurons in the parasubiculum can be broadly separated into three clusters based on their electrophysiological properties, and that each cluster corresponds to a different molecular marker. We demonstrate that while the PaS aligns structurally to some to general cortical principals, it also shows divergent features in particular in contrast to the MEC. This work will form an important basis for future studies working to disentangle the circuitry underlying memory and spatial navigation functions of the parasubiculum.SIGNIFICANCE STATEMENTWe identify the major neuron types in the parasubiculum using immunohistochemistry and electrophysiology, and determine their distribution throughout the PaS. We find that the neuronal composition of the parasubiculum differs considerably in comparison to the neighbouring medial entorhinal cortex. Both regions are involved in spatial navigation. Thus, our findings are of importance for unravelling the underlying circuitry of this process and for determining the role of the parasubiculum within this network.

Models of spatial representation in the medial entorhinal cortex

Thesis

Full-text available

Jul 2018

Tiziano D'Albis

Komplexe kognitive Funktionen wie Gedächtnisbildung, Navigation und Entscheidungsprozesse hängen von der Kommunikation zwischen Hippocampus und Neokortex ab. An der Schnittstelle dieser beiden Gehirnregionen liegt der entorhinale Kortex - ein Areal, das Neurone mit bemerkenswerten räumlichen Repräsentationen enthält: Gitterzellen. Gitterzellen sind Neurone, die abhängig von der Position eines Tieres in seiner Umgebung feuern und deren Feuerfelder ein dreieckiges Muster bilden. Man vermutet, dass Gitterzellen Navigation und räumliches Gedächtnis unterstützen, aber die Mechanismen, die diese Muster erzeugen, sind noch immer unbekannt. In dieser Dissertation untersuche ich mathematische Modelle neuronaler Schaltkreise, um die Entstehung, Weitervererbung und Verstärkung von Gitterzellaktivität zu erklären. Zuerst konzentriere ich mich auf die Entstehung von Gittermustern. Ich folge der Idee, dass periodische Repräsentationen des Raumes durch Konkurrenz zwischen dauerhaft aktiven, räumlichen Inputs und der Tendenz eines Neurons, durchgängiges Feuern zu vermeiden, entstehen könnten. Aufbauend auf vorangegangenen theoretischen Arbeiten stelle ich ein Einzelzell-Modell vor, das gitterartige Aktivität allein durch räumlich-irreguläre Inputs, Feuerratenadaptation und Hebbsche synaptische Plastizität erzeugt. Im zweiten Teil der Dissertation untersuche ich den Einfluss von Netzwerkdynamik auf das Gitter-Tuning. Ich zeige, dass Gittermuster zwischen neuronalen Populationen weitervererbt werden können und dass sowohl vorwärts gerichtete als auch rekurrente Verbindungen die Regelmäßigkeit von räumlichen Feuermustern verbessern können. Schließlich zeige ich, dass eine entsprechende Konnektivität, die diese Funktionen unterstützt, auf unüberwachte Weise entstehen könnte. Insgesamt trägt diese Arbeit zu einem besseren Verständnis der Prinzipien der neuronalen Repräsentation des Raumes im medialen entorhinalen Kortex bei.

Allocentric directional processing in the rodent and human retrosplenial cortex

Article

Full-text available

Mar 2014
FRONT HUM NEUROSCI

Head direction (HD) cells in the rodent brain have been investigated for a number of years, providing us with a detailed understanding of how the rodent brain codes for allocentric direction. Allocentric direction refers to the orientation of the external environment, independent of one's current (egocentric) orientation. The presence of neural activity related to allocentric directional coding in humans has also been noted but only recently directly tested. Given the current status of both fields, it seems beneficial to draw parallels between this rodent and human research. We therefore discuss how findings from the human retrosplenial cortex (RSC), including its "translational function" (converting egocentric to allocentric information) and ability to code for permanent objects, compare to findings from the rodent RSC. We conclude by suggesting critical future experiments that derive from a cross-species approach to understanding the function of the human RSC.

Weighted cue integration in the rodent head direction system

Article

Full-text available

Feb 2014
PHILOS T R SOC B

How the brain combines information from different sensory modalities and of differing reliability is an important and still-unanswered question. Using the head direction (HD) system as a model, we explored the resolution of conflicts between landmarks and background cues. Sensory cue integration models predict averaging of the two cues, whereas attractor models predict capture of the signal by the dominant cue. We found that a visual landmark mostly captured the HD signal at low conflicts: however, there was an increasing propensity for the cells to integrate the cues thereafter. A large conflict presented to naive rats resulted in greater visual cue capture (less integration) than in experienced rats, revealing an effect of experience. We propose that weighted cue integration in HD cells arises from dynamic plasticity of the feed-forward inputs to the network, causing within-trial spatial redistribution of the visual inputs onto the ring. This suggests that an attractor network can implement decision processes about cue reliability using simple architecture and learning rules, thus providing a potential neural substrate for weighted cue integration.

Rats With Hippocampal Lesions Can Learn a Place Response, but How Long Can They Retain It?

Article

Full-text available

Oct 2001

Juan M.J. Ramos

Previous research has shown that electrolytic hippocampal lesions do not affect the acquisition of a place response if a special training procedure is used. However, 24 days later, the hippocampal rats manifest a profound deficit in the retention of the spatial information (J. M. J. Ramos, 2000). The goal of the present study was, therefore, to investigate how long the hippocampal rats can retain a place response. Results showed that, 3 days after the end of the training, lesioned rats remembered as well as the control rats, but this was no longer true 6 or 12 days after the training. This retention deficit was not observed when the spatial information was acquired by means of a guidance strategy. These results suggest that, when a special training procedure is used, the hippocampus is not necessary for the learning of a place task but is required for the formation of long-term spatial memory.

Can hippocampal subfield measures supply information that could be used to improve the diagnosis of Alzheimer’s disease?

Article

Full-text available

Nov 2022
PLOS ONE

The diagnosis of Alzheimer’s disease (AD) needs to be improved. We investigated if hippocampal subfield volume measured by structural imaging, could supply information, so that the diagnosis of AD could be improved. In this study, subjects were classified based on clinical, neuropsychological, and amyloid positivity or negativity using PET scans. Data from 478 elderly Korean subjects grouped as cognitively unimpaired β-amyloid-negative (NC), cognitively unimpaired β-amyloid-positive (aAD), mild cognitively impaired β-amyloid-positive (pAD), mild cognitively impaired—specific variations not due to dementia β-amyloid-negative (CIND), severe cognitive impairment β-amyloid-positive (ADD+) and severe cognitive impairment β-amyloid-negative (ADD-) were used. NC and aAD groups did not show significant volume differences in any subfields. The CIND did not show significant volume differences when compared with either the NC or the aAD (except L-HATA). However, pAD showed significant volume differences in Sub, PrS, ML, Tail, GCMLDG, CA1, CA4, HATA, and CA3 when compared with the NC and aAD. The pAD group also showed significant differences in the hippocampal tail, CA1, CA4, molecular layer, granule cells/molecular layer/dentate gyrus, and CA3 when compared with the CIND group. The ADD- group had significantly larger volumes than the ADD+ group in the bilateral tail, SUB, PrS, and left ML. The results suggest that early amyloid depositions in cognitive normal stages are not accompanied by significant bilateral subfield volume atrophy. There might be intense and accelerated subfield volume atrophy in the later stages associated with the cognitive impairment in the pAD stage, which subsequently could drive the progression to AD dementia. Early subfield volume atrophy associated with the β-amyloid burden may be characterized by more symmetrical atrophy in CA regions than in other subfields. We conclude that the hippocampal subfield volumetric differences from structural imaging show promise for improving the diagnosis of Alzheimer’s disease.

Attractor-like Dynamics in the Subicular Complex

Article

Aug 2022

Distinct computations are performed at multiple brain regions during the encoding of spatial environments. Neural representations in the hippocampal, entorhinal and head direction (HD) networks during spatial navigation have been clearly documented, while the representational properties of the Subicular Complex (SC) are relatively under-explored, even though it has extensive anatomical connections with various brain regions involved in spatial information processing. We simultaneously recorded single units from different sub-regions of the SC in male rats while they ran clockwise on a centrally placed textured circular track (four different textures, each covering a quadrant), surrounded by six distal cues. The neural activity was monitored in standard sessions by maintaining the same configuration between the cues, while in cue manipulation sessions, the distal and local cues were either rotated in opposite directions to create a mismatch between them, or the distal cues were removed. We report a highly coherent neural representation of the environment and a robust coupling between the HD cells and the Spatial cells in the SC, strikingly different from previous reports of coupling between cells from co-recorded sites. Neural representations were (i) originally governed by the distal cues under local-distal cue-conflict conditions, (ii) controlled by the local cues in the absence of distal cues and (iii) governed by the cues that are perceived to be stable. We propose that such attractor-like dynamics in the SC might play a critical role in the orientation of spatial representations, thus providing a "reference map" of the environment for further processing by other networks.SIGNIFICANCE STATEMENTThe Subicular Complex (SC) receives major inputs from the entorhinal cortex and the hippocampus, and HD information directly from the HD system. Using cue-conflict experiments, we studied the hierarchical representation of the local and distal cues in the SC to understand its role in the cognitive map, and report a highly coherent neural representation with robust coupling between the HD cells and the spatial cells in different sub-regions of the SC exhibiting attractor-like dynamics unaffected by the cue manipulations, strikingly different from previous reports of coupling between cells from co-recorded sites. This unique feature may allow the SC to function as a single computational unit during the representation of space, which may serve as a reference map of the environment.

Spatial goal coding in the hippocampal formation

Article

Jan 2022
NEURON

The mammalian hippocampal formation contains several distinct populations of neurons involved in representing self-position and orientation. These neurons, which include place, grid, head direction, and boundary-vector cells, are thought to collectively instantiate cognitive maps supporting flexible navigation. However, to flexibly navigate, it is necessary to also maintain internal representations of goal locations, such that goal-directed routes can be planned and executed. Although it has remained unclear how the mammalian brain represents goal locations, multiple neural candidates have recently been uncovered during different phases of navigation. For example, during planning, sequential activation of spatial cells may enable simulation of future routes toward the goal. During travel, modulation of spatial cells by the prospective route, or by distance and direction to the goal, may allow maintenance of route and goal-location information, supporting navigation on an ongoing basis. As the goal is approached, an increased activation of spatial cells may enable the goal location to become distinctly represented within cognitive maps, aiding goal localization. Lastly, after arrival at the goal, sequential activation of spatial cells may represent the just-taken route, enabling route learning and evaluation. Here, we review and synthesize these and other evidence for goal coding in mammalian brains, relate the experimental findings to predictions from computational models, and discuss outstanding questions and future challenges.

Place Cells in Head-Fixed Mice Navigating a Floating Real-World Environment

Article

Full-text available

Feb 2021

The hippocampal place cell system in rodents has provided a major paradigm for the scientific investigation of memory function and dysfunction. Place cells have been observed in area CA1 of the hippocampus of both freely moving animals, and of head-fixed animals navigating in virtual reality environments. However, spatial coding in virtual reality preparations has been observed to be impaired. Here we show that the use of a real-world environment system for head-fixed mice, consisting of an air-floating track with proximal cues, provides some advantages over virtual reality systems for the study of spatial memory. We imaged the hippocampus of head-fixed mice injected with the genetically encoded calcium indicator GCaMP6s while they navigated circularly constrained or open environments on the floating platform. We observed consistent place tuning in a substantial fraction of cells despite the absence of distal visual cues. Place fields remapped when animals entered a different environment. When animals re-entered the same environment, place fields typically remapped over a time period of multiple days, faster than in freely moving preparations, but comparable with virtual reality. Spatial information rates were within the range observed in freely moving mice. Manifold analysis indicated that spatial information could be extracted from a low-dimensional subspace of the neural population dynamics. This is the first demonstration of place cells in head-fixed mice navigating on an air-lifted real-world platform, validating its use for the study of brain circuits involved in memory and affected by neurodegenerative disorders.

Local microcircuitry of parasubiculum shows distinct and common features of excitatory and inhibitory connectivity

Preprint

Full-text available

Dec 2020

The parasubiculum is located within the parahippocampal region, where it is thought to be involved in the processing of spatial navigational information. It contains a number of functionally specialised neuron types including grid cells, head direction cells and border cells, and provides input into layer 2 of the medial entorhinal cortex where grid cells are abundantly located. The local circuitry within the parasubiculum remains so far undefined but may provide clues as to the emergence of spatially tuned firing properties of neurons in this region. We used simultaneous patch-clamp recordings to determine the connectivity rates between the three major groups of neurons found in the parasubiculum. We find high rates of interconnectivity between the pyramidal class and interneurons, as well as features of pyramid to pyramid interactions indicative of a non-random network. The microcircuit that we uncover shares both similarities and divergences to those from other parahippocampal regions also involved in spatial navigation.

The subiculum and its role in focal epileptic disorders

Article

Nov 2020

The subicular complex (hereafter referred as subiculum), which is reciprocally connected with the hippocampus and rhinal cortices, exerts a major control on hippocampal outputs. Over the last three decades, several studies have revealed that the subiculum plays a pivotal role in learning and memory but also in pathological conditions such as mesial temporal lobe epilepsy (MTLE). Indeed, subicular networks actively contribute to seizure generation and this structure is relatively spared from the cell loss encountered in this focal epileptic disorder. In this review, we will address: (i) the functional properties of subicular principal cells under normal and pathological conditions; (ii) the subiculum role in sustaining seizures in in vivo models of MTLE and in in vitro models of epileptiform synchronization; (iii) its presumptive role in human MTLE; and (iv) evidence underscoring the relationship between subiculum and antiepileptic drug effects. The studies reviewed here reinforce the view that the subiculum represents a limbic area with relevant, as yet unexplored, roles in focal epilepsy.

Attractor-like spatial representations in the Subicular Complex network

Preprint

Full-text available

Feb 2020

Distinct computations are performed at multiple brain regions during encoding of the spatial environments. Neural representations in the hippocampal, entorhinal and head direction (HD) networks during spatial navigation have been clearly documented, while the representational properties of the Subicular Complex (SC) network is rather unexplored, even though it has extensive anatomical connections with various brain regions involved in spatial information processing. Here, we report a global cue controlled highly coherent representation of the cue-conflict environment in the SC network, along with strong coupling between HD cells and Spatial cells. We propose that the attractor dynamics in the SC network might play a critical role in orientation of the spatial representations, thus providing a reference map of the environment for further processing at other networks.

Hippocampal functional organization: A microstructure of the place cell network encoding space

Article

Apr 2019

A clue to hippocampal function has been the discovery of place cells, leading to the ‘spatial map’ theory. Although the firing attributes of place cells are well documented, little is known about the organization of the spatial map. Unit recording studies, thus far, have reported a low coherence between neighboring cells and geometric space, leading to the prevalent view that the spatial map is not topographically organized. However, the number of simultaneously recorded units is severely limited, rendering construction of the spatial map nearly impossible. To visualize the functional organization of place cells, we used the activity-dependent immediate-early gene Zif268 in combination with behavioral, pharmacological and electrophysiological methods, in mice and rats exploring an environment. Here, we show that in animals confined to a small part of a maze, principal cells in the CA1/CA3 subfields of the dorsal hippocampus immunoreactive (IR) for Zif268 adhere to a ‘cluster-type’ organization. Unit recordings confirmed that the Zif268 IR clusters correspond to active place cells, while blockade of NMDA R (which alters place fields) disrupted the Zif268 IR clusters. Contrary to the prevalent view that the spatial map consists of a non-topographic neural network, our results provide evidence for a ‘cluster-type’ functional organization of hippocampal neurons encoding for space.

Navigational Strategies and Their Neural Correlates

Article

Full-text available

Nov 2017

Animals depend on navigation to find food, water, mate(s), shelter, etc. Different species use diverse strategies that utilise forms of motion- and location-related information derived from the environment to navigate to their goals and back. We start by describing behavioural studies undertaken to unearth different strategies used in navigation. Then we move on to outline what we know about the brain area most associated with spatial navigation, namely the hippocampal formation. While doing so, we first briefly explain the anatomical connections in the area and then proceed to describe the neural correlates that are considered to play a role in navigation. We conclude by looking at how the strategies might interact and complement each other in certain contexts.

Flexible and Stable Value Coding Areas in Caudate Head and Tail Receive Anatomically Distinct Cortical and Subcortical Inputs

Article

Full-text available

Nov 2017

Anatomically distinct areas within the basal ganglia encode flexible- and stable-value memories for visual objects (Hikosaka et al., 2014), but an important question remains: do they receive inputs from the same or different brain areas or neurons? To answer this question, we first located flexible and stable value-coding areas in the caudate head (CDh) and caudate tail (CDt) of two rhesus macaque monkeys, and then injected different retrograde tracers into these areas of each monkey. We found that CDh and CDt received different inputs from several cortical and subcortical areas including temporal cortex, prefrontal cortex, cingulate cortex, amygdala, claustrum and thalamus. Superior temporal cortex and inferior temporal cortex projected to both CDh and CDt, with more CDt-projecting than CDh-projecting neurons. In superior temporal cortex and dorsal inferior temporal cortex, layers 3 and 5 projected to CDh while layers 3 and 6 projected to CDt. Prefrontal and cingulate cortex projected mostly to CDh bilaterally, less to CDt unilaterally. A cluster of neurons in the basolateral amygdala projected to CDt. Rostral-dorsal claustrum projected to CDh while caudal-ventral claustrum projected to CDt. Within the thalamus, different nuclei projected to either CDh or CDt. The medial centromedian nucleus and lateral parafascicular nucleus projected to CDt while the medial parafascicular nucleus projected to CDh. The inferior pulvinar and lateral dorsal nuclei projected to CDt. The ventral anterior and medial dorsal nuclei projected to CDh. We found little evidence of neurons projecting to both CDh and CDt across the brain. These data suggest that CDh and CDt can control separate functions using anatomically separate circuits. Understanding the roles of these striatal projections will be important for understanding how value memories are created and stored.

The representation of space in the brain

Article

Full-text available

Dec 2016
BEHAV PROCESS

The Functional Networks of Prepulse Inhibition: Neuronal Connectivity Analysis Based on FDG-PET in Awake and Unrestrained Rats

Article

Full-text available

Jul 2016

Prepulse inhibition (PPI) is a neuropsychological process during which a weak sensory stimulus (“prepulse”) attenuates the motor response (“startle reaction”) to a subsequent strong startling stimulus. It is measured as a surrogate marker of sensorimotor gating in patients suffering from neuropsychological diseases such as schizophrenia, as well as in corresponding animal models. A variety of studies has shown that PPI of the acoustical startle reaction comprises three brain circuitries for: (i) startle mediation, (ii) PPI mediation, and (iii) modulation of PPI mediation. While anatomical connections and information flow in the startle and PPI mediation pathways are well known, spatial and temporal interactions of the numerous regions involved in PPI modulation are incompletely understood. We therefore combined [18F]fluoro-2-deoxyglucose positron-emission-tomography (FDG-PET) with PPI and resting state control paradigms in awake rats. A battery of subtractive, correlative as well as seed-based functional connectivity analyses revealed a default mode-like network (DMN) active during resting state only. Furthermore, two functional networks were observed during PPI: Metabolic activity in the lateral circuitry was positively correlated with PPI effectiveness and involved the auditory system and emotional regions. The medial network was negatively correlated with PPI effectiveness, i.e., associated with startle, and recruited a spatial/cognitive network. Our study provides evidence for two distinct neuronal networks, whose continuous interplay determines PPI effectiveness in rats, probably by either protecting the prepulse or facilitating startle processing. Discovering similar networks affected in neuropsychological disorders may help to better understand mechanisms of sensorimotor gating deficits and provide new perspectives for therapeutic strategies.

Constraining the function of CA1 in associative memory models of the hippocampus

Thesis

Full-text available

May 2005

Kit D Longden

CA1 is the main source of afferents from the hippocampus, but the function of CA1 and its perforant path (PP) input remains unclear. In this thesis, Marr’s model of the hippocampus is used to investigate previously hypothesized functions, and also to investigate some of Marr’s unexplored theoretical ideas. The last part of the thesis explains the excitatory responses to PP activity in vivo, despite inhibitory responses in vitro. Quantitative support for the idea of CA1 as a relay of information from CA3 to the neocortex and subiculum is provided by constraining Marr’s model to experimental data. Using the same approach, the much smaller capacity of the PP input by comparison implies it is not a one-shot learning network. In turn, it is argued that the entorhinal-CA1 connections cannot operate as a short-term memory network through reverberating activity. The PP input to CA1 has been hypothesized to control the activity of CA1 pyramidal cells. Marr suggested an algorithm for self-organising the output activity during pattern storage. Analytic calculations show a greater capacity for self-organised patterns than random patterns for low connectivities and high loads, confirmed in simulations over a broader parameter range. This superior performance is maintained in the absence of complex thresholding mechanisms, normally required to maintain performance levels in the sparsely connected networks. These results provide computational motivation for CA3 to establish patterns of CA1 activity without involvement from the PP input. The recent report of CA1 place cell activity with CA3 lesioned (Brun et al., 2002. Science, 296(5576):2243-6) is investigated using an integrate-and-fire neuron model of the entorhinal-CA1 network. CA1 place field activity is learnt, despite a completely inhibitory response to the stimulation of entorhinal afferents. In the model, this is achieved using N-methyl-D-asparate receptors to mediate a significant proportion of the excitatory response. Place field learning occurs over a broad parameter space. It is proposed that differences between similar contexts are slowly learnt in the PP and as a result are amplified in CA1. This would provide improved spatial memory in similar but different contexts.

Subicular Place Cells Expand or Contract Their Spatial Firing Pattern to Fit the Size of the Environment in an Open Field but Not in the Presence of Barriers: Comparison With Hippocampal Place Cells

Article

Full-text available

Aug 1999

Patricia Sharp

Cells in the hippocampus and subiculum signal spatial location in fundamentally different ways. Specifically, hippocampal cells show environment-specific spatial patterns, whereas subicular cells show the same pattern in each environment. In this study, cell firing patterns were recorded in both a large square and in a smaller square located within the large square. For some groups, portions of the small square were left in place during exposure to the large square, thus forming partial barriers. Subicular cell patterns during exposure to the large square were expanded versions of those in the small square. Hippocampal cells were likely to change their pattern completely ("'remap") during exposure. However, when the barriers were left in place, cells in both areas retained the same pattern while rats were in the small square, regardless of whether they also had access to the entire large square area. Thus, subicular cells can change the size of their spatial pattern to fit the environment but will not do so across barriers.

Entorhinal Grid Cells and the Neural Basis of Navigation

Chapter

Mar 2008

This chapter reviews current knowledge about spatial representations in medial entorhinal cortex (MEC), its possible role in navigation, and how cell ensembles in MEC might contribute to the spatial component of hippocampal place cell representations. The discovery of a metric representation of self-location in MEC suggests that the primary function of the hippocampus is not the dynamic computation of location. Although the animal's position can be predicted from the collective firing of grid cell ensembles, it remains to be determined whether readout occurs within the entorhinal cortex or in one or several of its hippocampal or parahippocampal target structures. The contextual specificity of hippocampal representations suggests that during encoding, the hippocampus associates input from the self-motion-based coordinate system in MEC with other contextual information such as information from lateral entorhinal cortex (LEC). The possible recoding of spatial information from a positional code in MEC onto statistically independent, context-sensitive cell ensembles in high-capacity networks of the hippocampus is probably crucial for the successful storage of episodic memory.

Cocaine and amphetamine-regulated transcript and calcium binding proteins immunoreactivity in the subicular complex of the guinea pig

Article

Nov 2015

In this study we present the distribution and colocalization pattern of cocaine- and amphetamine-regulated transcript (CART) and three calcium-binding proteins: calbindin (CB), calretinin (CR) and parvalbumin (PV) in the subicular complex (SC) of the guinea pig. The subiculum (S) and presubiculum (PrS) showed higher CART-immunoreactivity (-IR) than the parasubiculum (PaS) as far as the perikarya and neuropil were concerned. CART- IR cells were mainly observed in the pyramidal layer and occasionally in the molecular layer of the S. In the PrS and PaS, single CART-IR perikarya were dispersed, however with a tendency to be found only in superficial layers. CART-IR fibers were observed throughout the entire guinea pig subicular neuropil. Double-labeling immunofluorescence showed that CART-IR perikarya, as well as fibers, did not stain positively for any of the three CaBPs. CART-IR fibers were only located near the CB-, CR-, PV- IR perikarya, whereas CART-IR fibers occasionally intersected fibers containing one of the three CaBPs. The distribution pattern of CART was more similar to that of CB and CR than to that of PV. In the PrS, the CART, CB and CR immunoreactivity showed a laminar distribution pattern. In the case of the PV, this distribution pattern in the PrS was much less prominent than that of CART, CB and CR. We conclude that a heterogeneous distribution of the CART and CaBPs in the guinea pig SC is in keeping with findings from other mammals, however species specific differences have been observed.

Quilichini, Sirota, Buzsáki 2010 J Neurosci

Data

Full-text available

Oct 2015

Investigating the functions of subregions within anterior hippocampus

Article

Full-text available

Oct 2015

Previous functional MRI (fMRI) studies have associated anterior hippocampus with imagining and recalling scenes, imagining the future, recalling autobiographical memories and visual scene perception. We have observed that this typically involves the medial rather than the lateral portion of the anterior hippocampus. Here, we investigated which specific structures of the hippocampus underpin this observation. We had participants imagine novel scenes during fMRI scanning, as well as recall previously learned scenes from two different time periods (one week and 30 min prior to scanning), with analogous single object conditions as baselines. Using an extended segmentation protocol focussing on anterior hippocampus, we first investigated which substructures of the hippocampus respond to scenes, and found both imagination and recall of scenes to be associated with activity in presubiculum/parasubiculum, a region associated with spatial representation in rodents. Next, we compared imagining novel scenes to recall from one week or 30 min before scanning. We expected a strong response to imagining novel scenes and 1-week recall, as both involve constructing scene representations from elements stored across cortex. By contrast, we expected a weaker response to 30-min recall, as representations of these scenes had already been constructed but not yet consolidated. Both imagination and 1-week recall of scenes engaged anterior hippocampal structures (anterior subiculum and uncus respectively), indicating possible roles in scene construction. By contrast, 30-min recall of scenes elicited significantly less activation of anterior hippocampus but did engage posterior CA3. Together, these results elucidate the functions of different parts of the anterior hippocampus, a key brain area about which little is definitely known.

Building a cognitive map by assembling multiple path integration systems

Article

Oct 2015
PSYCHON B REV

Ranxiao Frances Wang

Path integration and cognitive mapping are two of the most important mechanisms for navigation. Path integration is a primitive navigation system which computes a homing vector based on an animal's self-motion estimation, while cognitive map is an advanced spatial representation containing richer spatial information about the environment that is persistent and can be used to guide flexible navigation to multiple locations. Most theories of navigation conceptualize them as two distinctive, independent mechanisms, although the path integration system may provide useful information for the integration of cognitive maps. This paper demonstrates a fundamentally different scenario, where a cognitive map is constructed in three simple steps by assembling multiple path integrators and extending their basic features. The fact that a collection of path integration systems can be turned into a cognitive map suggests the possibility that cognitive maps may have evolved directly from the path integration system.

Unraveling the neural circuitry of sequence-based navigation using a combined fos imaging and computational approach

Article

Jun 2014

Benedicte M. Babayan

Spatial navigation is a complex function requiring the combination of external and self-motion cues to build a coherent representation of the external world and drive optimal behaviour directed towards a goal. This multimodal integration suggests that a large network of cortical and subcortical structures interacts with the hippocampus, a key structure in navigation. I have studied navigation in mice through this global approach and have focused on one particular type of navigation, which consists in remembering a sequence of turns, named sequence-based navigation or sequential egocentric strategy. This navigation specifically relies on the temporal organization of movements at spatially distinct choice points. We first showed that sequence-based navigation learning required the hippocampus and the dorsomedial striatum. Our aim was to identify the functional network underlying sequence-based navigation using Fos imaging and computational approaches. The functional networks dynamically changed across early and late learning stages. The early stage network was dominated by a highly inter-connected cortico-striatal cluster. The hippocampus was activated alongside structures known to be involved in self-motion processing (cerebellar cortices), in mental representation of space manipulations (retrosplenial, parietal, entorhinal cortices) and in goal-directed path planning (prefrontal-basal ganglia loop). The late stage was characterized by the emergence of correlated activity between the hippocampus, the cerebellum and the cortico-striatal structures. Conjointly, we explored whether path integration, model-based or model-free reinforcement learning algorithms could explain mice’s learning dynamics. Only the model-free system, as long as a retrospective memory component was added to it, was able to reproduce both the group learning dynamics and the individual variability observed in the mice. These results suggest that a unique model-free reinforcement learning algorithm was sufficient to learn sequence-based navigation and that the multiple structures this learning required adapted their functional interactions across learning.

Visual Landmark Information Gains Control of the Head Direction Signal at the Lateral Mammillary Nuclei

Article

Full-text available

Jan 2015

The neural representation of directional heading is conveyed by head direction (HD) cells located in an ascending circuit that includes projections from the lateral mammillary nuclei (LMN) to the anterodorsal thalamus (ADN) to the postsubiculum (PoS). The PoS provides return projections to LMN and ADN and is responsible for the landmark control of HD cells in ADN. However, the functional role of the PoS projection to LMN has not been tested. The present study recorded HD cells from LMN after bilateral PoS lesions to determine whether the PoS provides landmark control to LMN HD cells. After the lesion and implantation of electrodes, HD cell activity was recorded while rats navigated within a cylindrical arena containing a single visual landmark or while they navigated between familiar and novel arenas of a dual-chamber apparatus. PoS lesions disrupted the landmark control of HD cells and also disrupted the stability of the preferred firing direction of the cells in darkness. Furthermore, PoS lesions impaired the stable HD cell representation maintained by path integration mechanisms when the rat walked between familiar and novel arenas. These results suggest that visual information first gains control of the HD cell signal in the LMN, presumably via the direct PoS → LMN projection. This visual landmark information then controls HD cells throughout the HD cell circuit. Copyright © 2015 the authors 0270-6474/15/351354-14$15.00/0.

Otoconia-Deficient Mice Show Selective Spatial Deficits

Article

Oct 2014
HIPPOCAMPUS

Damage or inactivation of the vestibular system impairs performance on various spatial memory tasks, but few studies have attempted to disambiguate the roles of the semicircular canals and otolith organs in this performance. The present study tested the otolithic contribution to spatial working and reference memory by evaluating the performance of otoconia-deficient tilted mice on a radial arm maze and a Barnes maze. One radial arm maze task provided both intramaze and extramaze cues, whereas the other task provided only extramaze cues. The Barnes maze task provided only extramaze cues. On the radial arm maze, tilted mice performed similar to control mice when intramaze cues were available, but made more working and reference memory errors than control mice when only extramaze cues were available. On the Barnes maze task, control and tilted mice showed similar latency, distance, and errors during acquisition training. On the subsequent probe trial, both groups spent the greatest percentage of time in the goal quadrant, indicating they were able to use extramaze cues to guide their search. Overall, these results suggest signals originating in the otolith organs contribute to spatial memory, but are not necessary for all aspects of spatial performance. © 2014 Wiley Periodicals, Inc.

Functional correlates of the lateral and medial entorhinal cortex: Objects, path integration and local - Global reference frames

Article

Full-text available

Feb 2014
PHILOS T R SOC B

The hippocampus receives its major cortical input from the medial entorhinal cortex (MEC) and the lateral entorhinal cortex (LEC). It is commonly believed that the MEC provides spatial input to the hippocampus, whereas the LEC provides non-spatial input. We review new data which suggest that this simple dichotomy between 'where' versus 'what' needs revision. We propose a refinement of this model, which is more complex than the simple spatial-non-spatial dichotomy. MEC is proposed to be involved in path integration computations based on a global frame of reference, primarily using internally generated, self-motion cues and external input about environmental boundaries and scenes; it provides the hippocampus with a coordinate system that underlies the spatial context of an experience. LEC is proposed to process information about individual items and locations based on a local frame of reference, primarily using external sensory input; it provides the hippocampus with information about the content of an experience.

Hippocampal and subicular efferents and afferents of the peririnal, postrhinal, and entorhinal cortices of the rat

Article

Jul 2013

Available evidence suggests there is functional differentiation among hippocampal and parahippocampal subregions and along the dorsoventral (septotemporal) axis of the hippocampus. The aim of this study was to characterize and compare the efferent and afferent connections of perirhinal areas 35 and 36, postrhinal cortex, and the lateral and medial entorhinal areas (LEA and MEA) with dorsal and ventral components of the hippocampal formation (dentate gyrus, hippocampus cornu ammonis fields, and subiculum) as well as the presubiculum, and the parasubiculum. The entorhinal connections were also characterized with respect to the LEA and MEA dentate gyrus-projecting bands. In general, the entorhinal connections with the hippocampal formation are much stronger than the perirhinal and postrhinal connections. The entorhinal cortex projects strongly to all components of the hippocampal formation, whereas the perirhinal and postrhinal cortices project weakly and only to CA1 and the subiculum. In addition, the postrhinal cortex preferentially targets the dorsal CA1 and subiculum, whereas the perirhinal cortex targets ventral subiculum. Similarly, the perirhinal cortex receives more input from ventral hippocampal formation structures and the postrhinal cortex receives more input from dorsal hippocampal structures. The LEA and the MEA medial band are more strongly interconnected with ventral hippocampal structures, whereas the MEA lateral band is more interconnected with dorsal hippocampal structures. With regard to the presubiculum and parasubiculum, the postrhinal cortex and the MEA lateral band receive stronger input from the dorsal presubiculum and caudal parasubiculum. In contrast, the LEA and MEA medial bands receive stronger input from the ventral presubiculum and rostral parasubiculum.

Age dependent path Integration deficit in 5xFAD mice

Article

Feb 2024
BEHAV BRAIN RES

Electrophysiological recordings in rodents during spatial navigation: Single neuron recordings

Chapter

Jan 2023

Place cells in head-fixed mice navigating a floating real-world environment

Preprint

Full-text available

Oct 2020

The hippocampal place cell system in rodents has provided a major paradigm for the scientific investigation of memory function and dysfunction. Place cells have been observed in area CA1 of the hippocampus of both freely moving animals, and of head-fixed animals navigating in virtual reality environments. However, spatial coding in virtual reality preparations has been observed to be impaired. Here we show that the use of a real-world environment system for head-fixed mice, consisting of a track floating on air, provides some advantages over virtual reality systems for the study of spatial memory. We imaged the hippocampus of head-fixed mice injected with the genetically encoded calcium indicator GCaMP6s while they navigated circularly constrained or open environments on the floating platform. We observed consistent place tuning in a substantial fraction of cells, stable over multiple days, with remapping of place fields when the animal entered a different environment. Spatial information rates were within the range observed in freely moving mice. Manifold analysis indicated that spatial information could be extracted from a low-dimensional subspace of the neural population dynamics. This is the first demonstration of place cells in head-fixed mice navigating on an air-lifted real-world platform, validating its use for the study of brain circuits involved in memory and affected by neurodegenerative disorders.

Serotonin 5-HT1A Receptor-Mediated Reduction of Excitatory Synaptic Transmission in Layers II/III of the Parasubiculum

Article

Mar 2019
NEUROSCIENCE

Serotonin (5-HT) has important effects on cognitive function within the hippocampal region where it modulates membrane potential and excitatory and inhibitory synaptic transmission. Here, we investigated how 5-HT modulates excitatory synaptic strength in layers II/III of the parasubiculum in rat brain slices. Bath-application of 1 or 10 μM 5-HT resulted in a strong, dose-dependent, and reversible reduction in the amplitude of field excitatory postsynaptic potentials (fEPSPs) recorded in the parasubiculum. The 5-HT reuptake blocker citalopram (10 μM) also reduced fEPSP amplitudes, indicating that 5-HT released within the slice inhibits synaptic transmission. The reduction of fEPSPs induced by 5-HT was blocked by the 5-HT 1A receptor blocker NAN-190 (10 μM), but not by the 5-HT 7 receptor blocker SB-269970 (10 μM). Moreover, the 5-HT 1A agonist 8-OH-DPAT induced a reduction of fEPSP amplitude similar to that induced by 5-HT. The reduction was prevented by the 5-HT 1A receptor blocker NAN-190. The reduction in fEPSPs induced by either 5-HT or by 8-OH-DPAT was accompanied by an increase in paired-pulse ratio, suggesting that it is due mainly to reduced glutamate release. Our data suggest that the effects of serotonin on cognitive function may depend in part upon a 5-HT 1A -mediated reduction of excitatory synaptic transmission in the parasubiculum. This may also affect synaptic processing in the entorhinal cortex, which receives the major output projection of the parasubiculum.

Testing the Efficacy of Single-Cell Stimulation in Biasing Presubicular Head Direction Activity

Article

Full-text available

Feb 2018

To support navigation, the firing of head direction (HD) neurons must be tightly anchored to the external space. Indeed, inputs from external landmarks can rapidly reset the preferred direction of HD cells. Landmark stimuli have often been simulated as excitatory inputs from “visual cells” (encoding landmark information) to the HD attractor network; when excitatory visual inputs are sufficiently strong, preferred directions switch abruptly to the landmark location. In the present work, we tested whether mimicking such inputs via juxtacellular stimulation would be sufficient for shifting the tuning of individual presubicular HD cells recorded in passively rotated male rats. We recorded 81 HD cells in a cue-rich environment, and evoked spikes trains outside of their preferred direction (distance range, 11–178°). We found that HD tuning was remarkably resistant to activity manipulations. Even strong stimulations, which induced seconds-long spike trains, failed to induce a detectable shift in directional tuning. HD tuning curves before and after stimulation remained highly correlated, indicating that postsynaptic activation alone is insufficient for modifying HD output. Our data are thus consistent with the predicted stability of an HD attractor network when anchored to external landmarks. A small spiking bias at the stimulus direction could only be observed in a visually deprived environment in which both average firing rates and directional tuning were markedly reduced. Based on this evidence, we speculate that, when attractor dynamics become unstable (e.g., under disorientation), the output of HD neurons could be more efficiently controlled by strong biasing stimuli.

Spatial representation in the hippocampal formation: A history

Article

Oct 2017

Since the first place cell was recorded and the cognitive-map theory was subsequently formulated, investigation of spatial representation in the hippocampal formation has evolved in stages. Early studies sought to verify the spatial nature of place cell activity and determine its sensory origin. A new epoch started with the discovery of head direction cells and the realization of the importance of angular and linear movement-integration in generating spatial maps. A third epoch began when investigators turned their attention to the entorhinal cortex, which led to the discovery of grid cells and border cells. This review will show how ideas about integration of self-motion cues have shaped our understanding of spatial representation in hippocampal–entorhinal systems from the 1970s until today. It is now possible to investigate how specialized cell types of these systems work together, and spatial mapping may become one of the first cognitive functions to be understood in mechanistic detail.

Memory for Space, Time, and Episodes

Chapter

Jan 2017

Memory is one of the most studied cognitive abilities. Episodic memory, the capacity to remember personal experiences, has unquestionably increased the survival fitness of mammalian species, including humans. In fact, as animals live in a dynamic environment, the memory for unique experiences, organized in both space and time, has presumably evolved to complement other types of memories that are specialized in extracting generalities from multiple experiences. Here, we seek to review the behavioral approaches used to investigate spatial, temporal, and episodic memory in mammals and to provide insight into the specific brain structures and potential neuronal mechanisms underlying these capacities.

Parahippocampal and retrosplenial connections of rat posterior parietal cortex: Posterior parietal-parahippocampal connections

Article

Dec 2016
HIPPOCAMPUS

The posterior parietal cortex has been implicated in spatial functions, including navigation. The hippocampal and parahippocampal region and the retrosplenial cortex are crucially involved in navigational processes and connections between the parahippocampal/retrosplenial domain and the posterior parietal cortex have been described. However, an integrated account of the organization of these connections is lacking. Here we investigated parahippocampal connections of each posterior parietal subdivision and the neighboring secondary visual cortex using conventional retrograde and anterograde tracers as well as transsynaptic retrograde tracing with a modified rabies virus. The results show that posterior parietal as well as secondary visual cortex entertain overall sparse connections with the parahippocampal region but not with the hippocampal formation. The medial and lateral dorsal subdivisions of posterior parietal cortex receive sparse input from deep layers of all parahippocampal areas. Conversely, all posterior parietal subdivisions project moderately to dorsal presubiculum, whereas rostral perirhinal cortex, postrhinal cortex, caudal entorhinal cortex and parasubiculum all receive sparse posterior parietal input. This indicated that the presubiculum might be a major liaison between parietal and parahippocampal domains. In view of the close association of the presubiculum with the retrosplenial cortex, we included the latter in our analysis. Our data indicate that posterior parietal cortex is moderately connected with the retrosplenial cortex, particularly with rostral area 30. The relative sparseness of the connectivity with the parahippocampal and retrosplenial domains suggests that posterior parietal cortex is only a modest actor in forming spatial representations underlying navigation and spatial memory in parahippocampal and retrosplenial cortex. This article is protected by copyright. All rights reserved.

Environmental Anchoring of Head Direction in a Computational Model of Retrosplenial Cortex

Article

Full-text available

Nov 2016

Significance statement: The activity of head direction cells signals the direction of an animal's head relative to landmarks in the world. Although driven by internal estimates of head movements, head direction cells must be kept aligned to the external world by sensory inputs, which arrive in the reference frame of the sensory receptors. We present a computational model, which proposes that sensory inputs are correctly associated to head directions by virtue of a conjunctive representation of place and head directions in the retrosplenial cortex. The model allows for a stable head direction signal, even when the sensory input from nearby cues changes dramatically whenever the animal moves to a different location, and enables stable representations of head direction across connected environments.

Navigation and Episodic-Like Memory in Mammals

Chapter

Dec 2008

N.J. Fortin

Navigation and episodic memory are two of the most studied cognitive abilities in behavioral research. The capacity for efficient navigation is crucial to the survival of mammals; it allows them to optimally forage, search for mates, find shelter, and defend their territory, while conserving their energy and avoiding unnecessary exposure to predators. Episodic memory, the capacity to remember personal experiences, has unquestionably also increased the survival fitness of humans and of other mammals as well. In fact, as animals live in a continuously changing environment, the capacity for memory for unique experiences has presumably evolved to complement other types of memories specialized in extracting generalities from multiple experiences. For instance, the general knowledge that tigers are dangerous is adaptive, but remembering having seen a tiger near the river at dawn further benefits a potential prey. Navigation has been primarily studied in rodents, while episodic memory research has focused predominantly on humans. Although the two lines of research evolved rather independently for years, accumulating evidence indicates that both abilities share fundamental features and neural circuitry across mammalian species. The objectives of the present chapter are to review the behavioral approaches used to investigate navigation and episodic memory in different mammalian species, and to provide insight into the specific brain structures and potential neuronal mechanisms underlying both abilities.

Search For New Targets Of Deep Brain Stimulation For Epilepsy Treatment

Article

Full-text available

Mar 2016

Although clinical trials in refractory epilepsy are currently carried out, the field of deep brain stimulation (DBS) in epilepsy is still at its initial stage. Little is known about where, when and how to stimulate and what would be the short and long consequences. Animal studies might provide clinicians with new ideas regarding targets for DBS. Here an overview is given regarding old and new targets in rodent models of temporal lobe epilepsy. The evidence from animal models showed that stimulation of the subiculum – either in responsive or scheduled manner-is anticonvulsant in different seizure and epilepsy models, indicating that the subiculum might be a promising candidate for DBS targets. For the rest, the antiepileptic effects of low frequency stimulation were established mostly in kindling models. The presence of a critical time window in which stimulation was effective following after discharges on kindling acquisition, demonstrates that timing of DBS is an important factor for the anticonvulsant effects of DBS.

Time, space and hippocampal functions

Article

Jan 2003

C Holscher

The hippocampus is one of the most researched structures of the brain. Studies of lesions in humans, primates and rodents have suggested to some that the primary role of the hippocampus is to act as a temporary memory buffer which is required for the consolidation of long-term memory. The famous case study of patient H.M., in particular, seemed to suggest that the hippocampus was of crucial importance for memory formation. However, recordings of single neurons in freely moving rodents did not support this notion. In such recordings, neurons were found that were active predominately when the animal passed through a particular area in space. Consequently, these neurons were termed 'place cells' and a theory was developed that suggested that the hippocampus acts as a 'cognitive map' that is required for spatial orientation. It was then found that H.M. had significant damage to his temporal lobes that included the amygdala, rhinal cortices, and other areas. Further case studies and selective hippocampal lesions in primates resulted in much milder amnestic symptoms, and lesions of defined cortical areas in the temporal lobes showed that a number of functions previously attributed to the hippocampus were in fact linked to these areas. Further analysis of neuronal activity in the hippocampus showed that not only is spatial information represented there, but also additional information, such as speed of movement, direction of movement, match or non-match detection, olfactorial identification, and others. In addition, it was found that selective lesions of the hippocampus in rodents impaired spatial navigation and memory formation only mildly. Only simultaneous lesions of several cortical areas in conjunction with the hippocamus could reproduce the impairments and symptoms that were previously thought to be observed after hippocampal lesions alone. In conclusion it is proposed that information processing and memory formation is shared by several brain areas that act as a functional system. This review presents evidence from many different studies that the hippocampus is part of this system and plays a supportive role in associating complex multimodal information and laying down new memory traces. In addition, the concept of allocating specific functions (such as the development of a cognitive map) exclusively to the hippocampus is rejected.

Functional Architecture of the Rat Parasubiculum

Article

Full-text available

Feb 2016

Unlabelled: The parasubiculum is a major input structure of layer 2 of medial entorhinal cortex, where most grid cells are found. Here we investigated parasubicular circuits of the rat by anatomical analysis combined with juxtacellular recording/labeling and tetrode recordings during spatial exploration. In tangential sections, the parasubiculum appears as a linear structure flanking the medial entorhinal cortex mediodorsally. With a length of ∼5.2 mm and a width of only ∼0.3 mm (approximately one dendritic tree diameter), the parasubiculum is both one of the longest and narrowest cortical structures. Parasubicular neurons span the height of cortical layers 2 and 3, and we observed no obvious association of deep layers to this structure. The "superficial parasubiculum" (layers 2 and 1) divides into ∼15 patches, whereas deeper parasubicular sections (layer 3) form a continuous band of neurons. Anterograde tracing experiments show that parasubicular neurons extend long "circumcurrent" axons establishing a "global" internal connectivity. The parasubiculum is a prime target of GABAergic and cholinergic medial septal inputs. Other input structures include the subiculum, presubiculum, and anterior thalamus. Functional analysis of identified and unidentified parasubicular neurons shows strong theta rhythmicity of spiking, a large fraction of head-direction selectivity (50%, 34 of 68), and spatial responses (grid, border and irregular spatial cells, 57%, 39 of 68). Parasubicular output preferentially targets patches of calbindin-positive pyramidal neurons in layer 2 of medial entorhinal cortex, which might be relevant for grid cell function. These findings suggest the parasubiculum might shape entorhinal theta rhythmicity and the (dorsoventral) integration of information across grid scales. Significance statement: Grid cells in medial entorhinal cortex (MEC) are crucial components of an internal navigation system of the mammalian brain. The parasubiculum is a major input structure of layer 2 of MEC, where most grid cells are found. Here we provide a functional and anatomical characterization of the parasubiculum and show that parasubicular neurons display unique features (i.e., strong theta rhythmicity of firing, prominent head-direction selectivity, and output selectively targeted to layer 2 pyramidal cell patches of MEC). These features could contribute to shaping the temporal and spatial code of downstream grid cells in entorhinal cortex.

The Rodent Navigation Circuit

Chapter

Jan 2002

David S. Touretzky

Although the full extent of the circuitry involved in rodent navigation is not yet known, the major areas have been identified, and there are models of the computations thought to be taking place there. By adopting a computational approach to understanding navigation, we can deduce interactions that must occur between the rodent’s major navigational subsystems. Combined with anatomical knowledge, this provides strong constraints on theories of how the circuit works. In this chapter we will sketch a broad picture of the rodent navigation circuit and review current thinking about its anatomical realization. Earlier chapters in this book have discussed key components of the system; in this chapter, we will consider how these components interact.

Neural Representations Supporting Spatial Navigation and Memory

Article

Jan 2007

Neural representations of spatial information are substrates for behaviors that range from simple limb movements and basic locomotion to sophisticated navigation through complex environments. The processing of different types of spatial information, including the storage and recall of related neural representations, is integral to the ability to navigate through and interact with the external environment. Finding food, shelter, and potential mates requires an animal to develop an understanding of the spatial relationships between itself and numerous objects and goals within its environment. Two forms of information necessary for spatial navigation are the knowledge of one's location within an environment and directional heading, or orientation. This information is represented by neural activity distributed over several nuclei within the limbic system and neocortex. Furthermore, the ability to integrate, store, and recall these representations is essential for long-term survival strategies. This chapter discusses the neural representations of spatial location and orientation and how they can contribute to a spatial memory system.

Role of Estrogen in Regulation of Morphology and Synaptic Connectivity in Female Rat Subiculum

Conference Paper

Dec 2010
J Anat Soc India

Estrogen is reported to exert neuroprotective influences on the cornu ammonis as well as the dentate gyrus, two of the three components of the hippocampal memory system. Subiculum, the third and the output component of this system, plays a vital role in retrieval of previously learnt information (recall tasks). We undertook these studies to understand estrogen's role in regulating the synaptic connectivity, neurotransmission and neural degeneration in subiculum. For this, we used brains of aged (16-18 months) post-estropausal female Wistar rats, and compared them with those of adult (4-5 months) ovary-intact, ovariectomized, ovariectomized-vehicle treated and ovariectomized-estrogen treated rats. The vehicle (sesame oil) and estrogen therapy (17β estradiol, E2) were administered as daily subcutaneous injections (0.1 mg/kg of E2 in 0.1 ml vehicle) for 30 days. Serum estradiol assay was done to determine the levels of circulating serum estradiol levels. Brains were processed for Cresyl Violet, Golgi staining and Immunohistochemical studies [using anti-synaptophysin antibody]. Our results indicate that estrogen deficiency (induced by normal ageing or by ovariectomy) results in subicular neuronal degenerative changes, decreased synaptic connectivity and reduced dendritic arborization, most of which are reasonably reversed with estrogen replenishment. These studies suggest a unique role of estrogen in preventing and even reversing the senile neurodegenerative changes in female subiculum.

Architecture of spatial circuits in the hippocampal region

Article

Full-text available

Feb 2014
PHILOS T R SOC B

The hippocampal region contains several principal neuron types, some of which show distinct spatial firing patterns. The region is also known for its diversity in neural circuits and many have attempted to causally relate network architecture within and between these unique circuits to functional outcome. Still, much is unknown about the mechanisms or network properties by which the functionally specific spatial firing profiles of neurons are generated, let alone how they are integrated into a coherently functioning meta-network. In this review, we explore the architecture of local networks and address how they may interact within the context of an overarching space circuit, aiming to provide directions for future successful explorations.

A drivable bundle of microwires for collecting single-unit data from freely moving rats

Article

Full-text available

Jan 1984
PHYSIOL BEHAV

John L Kubie

A technique is described for making a sturdy, driveable electrode array of ten fine wires. This moveable array is a modification of a stationary electrode [4]. It has a number of notable advantages over other electrodes designed for recording single-unit activity in freely-moving small mammals. With this electrode many single cells can be recorded in each animal, cells can be held for many days, and recording quality is very good.

The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells

Article

Full-text available

Jun 1992

Hippocampal place cells in the rat are so named because they fire predominantly within circumscribed regions of the environment. This study describes the positional firing properties of cells afferent to hippocampal place cells, in superficial layers of medial entorhinal cortex (MEC). MEC cells in these layers project to the hippocampus via the perforant path and, along with lateral entorhinal cells, are the sole route by which cortical information reaches the hippocampus. MEC cells were recorded from rats while they retrieved pellets in simple geometric enclosures. The behavioral task as well as procedures for data collection and analysis were the same used in previous studies on hippocampal place cells (e.g., Muller et al., 1987) in order to facilitate the direct comparison between hippocampal and entorhinal cells. The firing patterns of MEC cells show pronounced locational variations reminiscent of hippocampal firing fields, but with a lower signal-to-noise ratio. While noisy, MEC firing patterns are stationary in time as evidenced by their reproducibility, and the improvement in spatial signal with long-duration recordings. Furthermore, MEC firing patterns are not due to variations in the rat's behavior. Taken together, these data show that the positional firing variations in MEC cells are due to the location-specificity of MEC cells. These and additional data lead us to conclude that location-specific information exists prior to the hippocampus. MEC cells are similar to hippocampal place cells in that their firing can be controlled by the rotation of a visual cue (a white card attached to the wall), but is not disrupted by removing the cue. An important difference between hippocampal and entorhinal cells was seen when the shape of the recording chamber was changed. In the transition from a cylinder to an equal-area square of similar appearance, MEC firing patterns topologically transformed (or "stretched") while those of hippocampal place cells changed to an unpredictable pattern. We conclude that the positional firing of MEC cells is more "sensory bound" than hippocampal cells, and that the ability to discriminate different environments, while present in the hippocampus, is not yet present in its input from MEC.

The connections of presubiculum and parasubiculum in the rat

Article

Full-text available

Jul 1990
BRAIN RES

The present study describes the differences and similarities between the connections of the presubiculum and parasubiculum based on retrograde and anterograde tracing experiments. The results demonstrate that both areas have several similar afferent connections, particularly those from subcortical areas such as the claustrum, diagonal band of Broca, anterior thalamus, nucleus reuniens, locus coeruleus, and raphe nuclei. Both subicular areas also are innervated by axons originating in the ipsilateral and contralateral entorhinal cortex, presubiculum, and parasubiculum. In contrast to these similarities, most axons innervating the presubiculum originate in the lateral dorsal thalamic nucleus, the claustrum, and the contralateral presubiculum. Conversely, the parasubiculum is innervated primarily by axons that originate in area CA1 of the hippocampus, the basolateral nucleus of the amygdala, and the contralateral presubiculum and parasubiculum. The major efferent projection from the presubiculum and parasubiculum courses bilaterally to the medial entorhinal cortex; however, the results of the present study confirm previous suggestions that presubicular axons terminate almost exclusively in layers I and III, whereas parasubicular axons innervate layer II. The presubiculum also projects to the anteroventral and laterodorsal nuclei of the thalamus, and the lateral ventral portion of the medial mammillary nucleus, whereas the parasubiculum projects prominently to the anterodorsal nucleus of the thalamus, the contralateral presubiculum and parasubiculum, and the lateral dorsal segment of the medial mammillary nucleus. Thus despite some similarities, the major connections of presubiculum and parasubiculum are distinct from one another and distinct from the projections of the adjacent subiculum and postsubiculum. These results suggest that the subicular cortex is considerably more complex than previously envisioned and indicate that each segment may subserve a distinct role in the processing of information by the hippocampal formation.

Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations

Article

Full-text available

Mar 1990

Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis

Article

Full-text available

Mar 1990

This paper is a study of the behavioral and spatial firing correlates of neurons in the rat postsubiculum. Recordings were made from postsubicular neurons as rats moved freely throughout a cylindrical chamber, where the major cue for orientation was a white card taped to the inside wall. An automatic video/computer system monitored cell discharge while simultaneously tracking the position of 2 colored light emitting diodes (LEDs) secured to the animal's head. The animal's location was calculated from the position of one of the LEDs and head direction in the horizontal plane calculated from the relative positions of the 2 LEDs. Approximately 26% of the cells were classified as head-direction cells because they discharged as a function of the animal's head direction in the horizontal plane, independent of the animal's behavior, location, or trunk position. For each head-direction cell, vectors drawn in the direction of maximal firing were parallel throughout the recording chamber and did not converge toward a single point. Plots of firing rate versus head direction showed that each firing-rate/head-direction function was adequately described by a triangular function. Each cell's maximum firing rate occurred at only one (the preferred) head direction; firing rates at head directions on either side of the preferred direction decreased linearly with angular deviation from the preferred direction. Results from 24 head-direction cells in 7 animals showed an equal distribution of preferred firing directions over a 360 degrees angle. The peak firing rate of head-direction cells varied from 5 to 115 spikes/sec (mean: 35). The range of head-direction angles over which discharge was elevated (directional firing range) was usually about 90 degrees, with little, if any, discharge at head directions outside this range. Quantitative analysis showed the location of the animal within the cylinder had minimal effect on directional cell firing. For each head-direction cell, the preferred direction, peak firing rate, and directional firing range remained stable for days. These results identify a new cell type that signals the animal's head direction in its environment.

Spatial firing properties of hippocampal θ cells

Article

Full-text available

May 1990

Previous studies have shown that complex-spike cells, the most common cell type recorded in the hippocampus of freely moving rats, have the property of spatial firing--that is, a cell will fire rapidly only when the animal is in a particular part of its environment (O'Keefe and Dostrovsky, 1971). In the current study, we analyze the spatial firing of theta cells, the second major class of cells in the hippocampus, which are thought to correspond to nonpyramidal neurons (Fox and Ranck, 1975, 1981). Our purposes were to extend findings from earlier spatial analyses (McNaughton et al., 1983; Christian and Deadwyler, 1986), and to determine whether the spatial firing is cell specific and independent of behavior. Theta cells were recorded from rats in a cylindrical enclosure using techniques previously used for the analysis of spatial firing in complex-spike cells (Muller et al., 1987). The spatial firing patterns of individual neurons appeared as a complex surface with several regions of high and low firing. The ratio of firing from high- to low-rate regions averaged 2.5. These spatial firing patterns were smooth and reproducible, but less so than for complex-spike cells. When a cue card on the wall was moved, theta cell firing patterns remained in register with the cue. Two analyses were performed to determine whether spatial firing patterns were secondary to spatial distributions of behavior. When only locomotor data segments were selected, spatial variations were more clear-cut. In an attempt to test whether theta cells had cell-specific patterns of firing, pairs of theta cells were recorded simultaneously. On all occasions, the firing distribution for each of the cells in a pair was clearly distinctive. These findings support the conclusions that theta cell activity contains a spatial signal that is cell specific and not secondary to other firing correlates.

The firing of hippocampal place cells predicts the future position of freely moving rats

Article

Full-text available

Jan 1990

Direct observation and automatic, video-based methods reveal that a large fraction of hippocampal pyramidal neurons recorded from freely moving rats behave as "place cells"; the firing of each place cell occurs almost exclusively when the rat is in a restricted part of its current environment. In earlier work, 2-dimensional firing distributions for place cells over the apparatus area were made under the assumption that the correct location for each spike was the animal's position at the instant that the spike was fired. Spatial firing distributions generated in this way often have a very simple structure, in which the single region of intense activity has a just one maximum, and where the rate decreases monotonically in all directions away from the maximum. We will refer to patterns of this sort as "ideal." We describe how the spatial firing pattern is altered by assigning spikes to positions earlier or later than the instant at which they were fired. Spatial firing distributions were generated for a range of constant displacements of the spike time-series against the position time series. Three quantitative measures were used to estimate the extent to which the spatial firing pattern at different "spike/position shifts" approximated the ideal pattern. The 3 measures are in agreement that spikes must precede the animal's position by about 120 msec for the spatial firing pattern to be closest to the ideal. These results suggest that hippocampal unit activity predicts the animal's future location on a short time scale.

The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells

Article

Full-text available

Aug 1987

Using the techniques set out in the preceding paper (Muller et al., 1987), we investigated the response of place cells to changes in the animal's environment. The standard apparatus used was a cylinder, 76 cm in diameter, with walls 51 cm high. The interior was uniformly gray except for a white cue card that ran the full height of the wall and occupied 100 degrees of arc. The floor of the apparatus presented no obstacles to the animal's motions. Each of these major features of the apparatus was varied while the others were held constant. One set of manipulations involved the cue card. Rotating the cue card produced equal rotations of the firing fields of single cells. Changing the width of the card did not affect the size, shape, or radial position of firing fields, although sometimes the field rotated to a modest extent. Removing the cue card altogether also left the size, shape, and radial positions of firing fields unchanged, but caused fields to rotate to unpredictable angular positions. The second set of manipulations dealt with the size and shape of the apparatus wall. When the standard (small) cylinder was scaled up in diameter and height by a factor of 2, the firing fields of 36% of the cells observed in both cylinders also scaled, in the sense that the field stayed at the same angular position and at the same relative radial position. Of the cells recorded in both cylinders, 52% showed very different firing patterns in one cylinder than in the other. The remaining 12% of the cells were virtually silent in both cylinders. Similar results were obtained when individual cells were recorded in both a small and a large rectangular enclosure. By contrast, when the apparatus floor plan was changed from circular to rectangular, the firing pattern of a cell in an apparatus of one shape could not be predicted from a knowledge of the firing pattern in the other shape. The final manipulations involved placing vertical barriers into the otherwise unobstructed floor of the small cylinder. When an opaque barrier was set up to bisect a previously recorded firing field, in almost all cases the firing field was nearly abolished. This was true even though the barrier occupied only a small fraction of the firing field area. A transparent barrier was effective as the opaque barrier in attenuating firing fields. The lead base used to anchor the vertical barriers did not affect place cell firing.(ABSTRACT TRUNCATED AT 400 WORDS)

Spatial firing pattern of hippocampal complex-spike cells in a fixed environment

Article

Full-text available

Aug 1987

A TV/computer technique was used to simultaneously track a rat's position in a simple apparatus and record the firing of single hippocampal complex-spike neurons. The primary finding is that many of these neurons behave as "place cells," as first described by O'Keefe and Dostrovsky (1971) and O'Keefe (1976). Each place cell fires rapidly only when the rat is in a delimited portion of the apparatus (the cell's "firing field"). In agreement with O'Keefe (1976) and many other authors, we have seen that the firing of place cells is highly correlated with the animal's position and is remarkably independent of other aspects of the animal's behavioral state. Several properties of firing fields were characterized. Firing fields are stable over long time intervals (days) if the environment is constant. They come in several shapes when the animal is in a cylindrical apparatus; moreover, the set of field shapes is different when the animal is in a rectangular apparatus. It also seems that a single cell may have more than one field in a given apparatus. By collecting a sample of 40 place cells in a fixed environment, it has been possible to describe certain features of the place cell population, including the spatial distribution of fields within the apparatus, the average size of fields, and the "intensity" of fields (as measured by maximum firing rate). We also tested the hypothesis that the firing rate of each place cell signals the animal's distance from a point (the field center) so that a weighted average of the firing of the individual cells encodes the animal's position within the apparatus. The animal's position, calculated according to this "distance hypothesis," is systematically different from the animal's true position; this implies that the hypothesis in its simplest form is wrong.

Head direction cells recorded in the ATN of freely moving rats

Article

Full-text available

Feb 1995

Jeffrey S Taube

Previous studies have identified neurons in the postsubiculum which discharge as a function of the animal's head direction in the horizontal plane, independent of its behavior and location in the environment. Anatomical studies have shown that the postsubiculum contains reciprocal connections with the anterior thalamic nuclei (ATN). In order to determine how the head direction (HD) cell signal is processed in the brain, single-unit recordings were monitored in the ATN of freely moving rats in order to characterize their behavioral and spatial correlates. Animals were trained to retrieve food pellets thrown randomly into a cylindrical apparatus containing a single orientation cue. Single unit recordings in the ATN showed that approximately 60% of the recorded cells discharged in relation to the animal's head direction in the horizontal plane. Observation of the animal and quantitative analyses showed that HD cell firing was not dependent on the animal's behavior, trunk position, linear speed, angular head velocity, or location in the environment. Most of these cells were localized to the anterior dorsal thalamic nucleus. Each HD cell contained only one head direction at which the cell discharged maximally and the firing rate decreased linearly away from this preferred direction. The preferred firing directions from all cells recorded were distributed over a 360 degrees range. Quantitative analysis showed that these cells contained similar discharge parameters (peak firing rate, directional firing range) to values reported previously for postsubicular HD cells (Taube et al., 1990a). Experiments involving rotation of the orientation cue showed that the preferred firing direction could be controlled by a salient visual cue. In contrast to postsubicular HD cells, passive rotation of a restrained animal showed that most ATN HD cells ceased discharging when the animal's head was oriented in the preferred direction. These findings demonstrate the presence of HD cells in the ATN and indicate the potential importance of this area for spatial navigation. The origin of the head direction signal is discussed and it is concluded that because of the presence of reciprocal connections between the postsubiculum and the ATN, further studies are required in order to determine the direction in which this head-directional information is flowing. Finally, ATN HD cells differ from postsubicular HD cells by appearing to require volitional motoric input.

Place cells in the ventral hippocampus of rats

Article

Full-text available

Nov 1994
NEUROREPORT

Many cells recorded from the dorsal hippocampus of freely moving rats are intensely active only when the rat's head is in a particular part of its environment. For this reason, such units are called 'place cells'. We have investigated whether place cells are also found in the ventral hippocampus. Recordings were made from ventral hippocampal units while rats chased food pellets in a cylindrical arena. The rat's position was simultaneously recorded by tracking a light on the rat's head. Our data show the existence of cells in the ventral hippocampus whose positional firing patterns and electrophysiological properties are very similar to those of dorsal hippocampal place cells.

Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat

Article

Full-text available

Jan 1995

The septal and temporal poles of the hippocampus differ markedly in their anatomical and neurochemical organization. Although it is well established that the internal representation of space is a fundamental function of hippocampal neurons, most of what is known about spatial coding in the hippocampus of freely moving animals has come from recordings from the dorsal one-third (largely for technical convenience). The present study therefore compared the spatial selectivity of CA1 neurons in the dorsal and ventral hippocampi of rats during performance of a food reinforced, random search task in a square chamber containing simple visual landmarks. Neural activity was recorded in the dorsal and ventral hippocampi of opposite hemispheres in the same rats, in many cases simultaneously. As in dorsal hippocampus, ventral CA1 units could be classified as "complex spike" (pyramidal) cells or "theta" interneurons. Both dorsal and ventral theta cells fired at relatively high rates and with low spatial selectivity in the apparatus. Of the population of complex spike cells in the ventral hippocampus, a significantly smaller number had "place fields" than in the dorsal hippocampus, and the average spatial selectivity was of significantly lower resolution than that found among dorsal hippocampal complex spike cells. Thus, a septotemporal difference of spatial selectivity was found in the CA1 field of the rat hippocampus, complementing many other anatomical and neuropharmacological studies. A number of possible functional interpretations can be suggested from these results, including a computational advantage of representing space at different scales or a preeminence of essentially nonspatial information processing in the ventral hippocampus.

On the directional properties of hippocampal place cells

Article

Full-text available

Jan 1995

Using a two-spot tracking system that allowed measurements of the direction of a rat's head in the environment as well as the position of the rat's head, we investigated whether hippocampal place cells show true direction-specific as well as location-specific firing. Significant modulations of firing rate by head direction were seen for most cells while rats chased food pellets in a cylindrical apparatus. It was possible, however, to account quantitatively for directional modulation with a simple scheme that we refer to as the "distributive hypothesis." This hypothesis assumes that firing is ideally location specific, and that all directional firing modulations are due to differences in the time that the rat spends in different portions of the firing field of the place cell in different head direction sectors. When the distributive hypothesis is put into numeric form, the directional firing profiles that it predicts are extremely similar to the observed directional firing profiles, strongly suggesting that there is no intrinsic directional specificity of place cell firing in the cylinder. Additional recordings made while rats ran on an eight-arm maze reveal that many firing fields on the arms are polarized; the cell discharges more rapidly when the rat runs in one direction than the other on the maze. This result provides an independent confirmation of the findings of McNaughton et al. (1983). For fields that appear to be polarized by inspecting firing rate maps of the raw data, the magnitude of directional firing variations is greater than predicted by the distributive hypothesis. By comparison with postsubicular head direction cells, it is shown that the distributive prediction of weaker-than-observed directional firing is expected if there is a true directional firing component. A major conclusion reached from recording in both environments is that the directional firing properties of hippocampal place cells are variable and not fixed; this is true of individual units as well as of the population.

Spatial Correlates of Firing Patterns of Single Cells in the Subiculum of the Freely Moving Rat

Article

Full-text available

May 1994

Hippocampal lesions cause spatial learning deficits, and single hippocampal cells show location-specific firing patterns, known as place fields. This suggests the hippocampus plays a critical role in navigation by providing an ongoing indication of the animal's momentary spatial location. One question that has received little attention is how this locational signal is used by downstream brain regions to orchestrate actual navigational behavior. As a first step, we have examined the spatial firing correlates of cells in the dorsal subiculum as rats navigate in an open-field, pellet-searching task. The subiculum is one of the few major output zones for the hippocampus, and it, in turn, projects to numerous other brain areas, each thought to be involved in various learning and memory functions. Most subicular cells showed a robust locational signal. The patterns observed were different from those in the hippocampus, however, in that cells tended to fire throughout much of the environment, but showed graded, location-related rate modulation, such that there were some localized regions of high firing and other regions with relatively low firing. There were slight quantitative differences between the proximal (adjacent to the hippocampus) and distal (farther from the hippocampus) subicular regions, with distal cells showing slightly higher average firing rates, spatial signaling, and firing field size. This was of interest since these two regions have different efferent connections. Examination of spike trains allowed classification of cells into bursting, nonbursting, and theta (putative interneuron) categories, and this is similar to subicular cell types identified in vitro. Interestingly, the bursting and nonbursting types did not differ detectably in spatial firing properties, suggesting that differences in intrinsic membrane properties do not necessitate differences in coding of environmental inputs. The results suggest that the subiculum transmits a robust, highly distributed spatial signal to each of its projection areas, and that this signal is transmitted in both a bursting and nonbursting mode.

Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats

Article

Full-text available

Oct 1993

The hippocampal formation has been extensively studied for its special role in visual spatial learning and navigation. To ascertain the nature of the associations made, or computations performed, by hippocampus, it is important to delineate the functional contributions of its afferents. Therefore, single units were recorded in the lateral dorsal nucleus of the thalamus (LDN) as rats performed multiple trials on a radial maze. Many LDN neurons selectively discharged when an animal's head was aligned along particular directions in space, irrespective of its location in the test room. These direction-sensitive cells were localized to the dorsal aspect of the caudal two-thirds of the LDN, the site of innervation by retinal recipient pretectal and intermediate/deep-layer superior colliculus cells (Thompson and Robertson, 1987b). The directional specificity and preference of LDN cells were disrupted if rats were placed on the maze in darkness. If the room light was then turned on, the original preference was restored. If the light was again turned off, directional firing was maintained briefly. Normal directional firing lasted about 2-3 min. After this time, the directional preference (but not specificity) appeared to "rotate" systematically in either the clockwise or counterclockwise direction. The duration of normal directional discharge patterns in darkness could be extended to 30 min by varying the behavior of the animal. LDN cells required visual input to initialize reliable directional firing. After the rat viewed the environment, directional specificity was maintained in the absence of visual cues. Maximal directional firing was achieved only when the rat viewed the entire test room, and not just the scene associated with the directional preference of the cell. Thus, contextual information seems important. Also, a significant correlation was found between directional specificity and errors made on the maze during acquisition of the task. It was concluded that the LDN may pass on to the hippocampal formation directional information that is not merely a reflection of current sensory input. As such, the LDN may serve an important integrative function for limbic spatial learning systems.

Spatial and behavioral correlates of striatal neurons in rats performing a self-initiated navigation task

Article

Full-text available

Sep 1993

Sidney I Wiener

To investigate the spatial and behavioral correlates of striatal neurons during displacement movements, the rostromedial dorsal striata (AP 1.0-2.2, ML 1.5-2.0) of five rats were surgically implanted with advanceable bundles of fine wire electrodes. After recovery, the rats were deprived of water and trained in a square-walled open field in a dark room. The behavioral task required alternating visits to water reservoirs in the center and in the four corners. A certain corner contained the first reward for each trial; after this reward, a cue card appeared in this corner for the rest of the trial. The firing rates of striatal units were compared as the rat moved between the center and the four corners of the arena. Analyses were made of 30 units. Eight of these had firing rates that significantly increased or decreased by 62-480% while the rat was in one or more quadrants of the arena. Six of these manifested such firing rate changes only as the rat performed certain behavioral sequences in the quadrant. Three other units fired as the rat's head was in a certain orientation relative to the arena walls, in all parts of the arena. To determine the principal controlling cues and hence the frame of reference of spatial selectivity of these units, the arena, while the rat was still inside, was rotated in total darkness. The first water reward was then presented at the same position relative to the outside room as before the rotation. The cue card was then illuminated in this corner as a visual cue for the extra-arena reference frame. All 11 neurons demonstrated spatial selectivity that rotated with the arena; thus, this activity was in the frame of reference of the arena and was not controlled by the visual cue. Six other units fired at rates up to six times their resting discharge or stopped firing completely in synchrony with initiation or execution of displacement movements, and two of these were also location selective. Four other units were silent as the rat performed the task, but fired tonically following arena rotations or other interruptions of the session, independent of the rat's location or movements. Nine analyzed units had very low firing rates (< 1 impulse/sec) and showed no discernible changes in activity as the rat performed the task. These patterns of unit activity indicate that fundamental informational components required for navigation are coded in the striatum.(ABSTRACT TRUNCATED AT 400 WORDS)

The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat

Article

Dec 1971
BRAIN RES

Studies of single neurons in dorsal hippocampal formation and septum in unrestrained rats. Part I. Behavioral correlates and firing repertoires. Part II. Hippocampal slow waves and theta cell firing during bar pressing and other behaviors

Article

Nov 1973

J.B. Ranck Jr

Development of the nervous system, second edition

Article

Jun 2006
PHYSIOL BEHAV

Michael P Matise

Head-direction cells in the rat posterior cortex

Article

Sep 1994

We examined the behavioral modulation of head-directional information processing in neurons of the rat posterior cortices, including the medial prestriate (area Oc2M) and retrosplenial cortex (areas RSA and RSG). Single neurons were recorded in freely moving rats which were trained to perform a spatial working memory task on a radial-arm maze in a cue-controlled room. A dual-light-emitting diode (dual-LED) recording headstage, mounted on the animals' heads, was used to track head position and orientation. Planar modes of motion, such as turns, straight motion, and nonlocomotive states, were categorized using an objective scheme based upon the differential contributions of movement parameters, including linear and angular velocity of the head. Of 662 neurons recorded from the posterior cortices, 41 head-direction (HD) cells were identified based on the criterion of maintained directional bias in the absence of visual cues or in the dark. HD cells constituted 7 of 257 (2.7%) cells recorded in Oc2M, 26 of 311 (8.4%) cells in RSA, and 8 of 94 (8.5%) cells in RSG. Spatial tuning of HD cell firing was modulated by the animal's behaviors in some neurons. The behavioral modulation occurred either at the preferred direction or at all directions. Moreover, the behavioral selectivity was more robust for turns than straight motions, suggesting that the angular movements may significantly contribute to the head-directional processing. These behaviorally selective HD cells were observed most frequently in Oc2M (4/7, 57%), as only 5 of 26 (19%) of RSA cells and none of the RSG cells showed behavioral modulation. These data, taken together with the anatomical evidence for a cascade of projections from Oc2M to RSA and thence to RSG, suggest that there may be a simple association between movement and head-directionality that serves to transform the egocentric movement representation in the neocortex into an allocentric directional representation in the periallocortex.

Characteristics of sparsely encoded associative memory

Article

Dec 1989
NEURAL NETWORKS

Shun-ichi Amari

Characteristics of an autocorrelation or crosscorrelation associative memory largely depend on how items are encoded in pattern vectors to be stored. When most of the components of encoded patterns to be stored are 0 and only a small ratio of the components are 1, the encoding scheme is said to be sparse. The memory capacity and information capacity of a sparsely encoded associative memory are analyzed in detail, and are proved to be in proportion of , n being the number of neurons, which is very large compared to the ordinary non-sparse encoding scheme of about 0.15n. Moreover, it is proved that the sparsely encoded associative memory has a large basin of attraction around each memorized pattern, when and only when an activity control mechanism is attached to it.

Hippocampal Place Units in the freely moving rat: Why they fire where they fire

Article

May 1978

Place units in the dorsal hippocampus of the freely-moving rat signal the animal's position in an environment (place field). In the present experiments, thirty four place units were recorded in two different environments: one, a small platform where the rat had received neither training nor reward; the other, an elevated T-maze inside a set of black curtains where the rat had been trained on a place discrimination. The places within the curtained enclosure were specified by four cues (a light, a card, a fan, and a buzzer) in addition to the food. Other cues were eliminated by rotating the maze and the four controlled cues relative to the external world from trial-to-trial. Some units had place fields in both environments while others only had a place field in one. No relationship could be seen between the place fields of units with fields in both environments. All twelve units tested extensively in the controlled enclosure had place fields related to the controlled cues. Probe experiments in which only some of the controlled cues were available showed that some of these units were being excited by one or two cues while others were influenced in a more complex way. The fields of these latter units were maintained by any two of the 4 cues and were due to inhibitory influences which suppressed the unit firing over the rest of the maze.

Projections from the amygdaloid complex and adjacent olfactory structures to the entorhinal cortex and to the subiculum in the rat and cat

Article

Apr 1977

Axonal projections are described from the lateral and hasolateral nuclei of the amygdaloid complex, and from the overlying periamygdaloid and pre-piriform cortices and the endopiriform nucleus, to the lateral entorhinal area, the ventral part of the subiculum, and the parasubiculum in the cat and rat. All of these projections have well-defined laminar patterns of termination, which are complementary to those of other projections to the same structure. Based on these results, and on cytoarchitectonic distinctions, the lateral entorhinal area has been divided into dorsal, ventral, and ventromedial subdivisions. The olfactory bulb and prepiriform cortex project to layers IA and IB, respectively, of all three subdivisions, but the lateral amygdaloid nucleus has a restricted projection to layer 111 of the ventral subdivision only. The periamygdaloid cortex projects to layer II of the ventromedial and adjoining parts of the ventral subdivisions. The ventral part of the subiculum receives fibers from the posterior division of the hasolateral nucleus, which terminate in the cellular layer and the deep half to one-third of the plexiform layer. The periamygdaloid cortex and the endopiriform nucleus also project to the same part of the subiculum, but these fibers terminate in the outer part of the plexiform layer. None of these projections extend into the dorsal part of the subiculum. The posterior division of the basolateral nucleus also projects to the posterodorsal part of the parasubiculum (“parasubiculum a” of Blackstad, 1956). These fibers end in the deeper part of the plexiform layer and the superficial part of the cellular layer.

Medial septal modulation of entorhinal single unit activity in anesthetized and freely moving rats

Article

Feb 1992
BRAIN RES

Reversible inactivation of the medial septal area results in a spatial memory impairment and selective disruption of hilar/CA3, but not CA1, location-specific discharge. The present study examined the possibility that such septal deafferentation produces effects on hippocampal function by altering physiological properties of the primary input and output structures for hippocampus, the entorhinal cortex and the subiculum, respectively. Single unit activity of hippocampal, entorhinal, and subicular cells was recorded before, during, and after septal injection of lidocaine in anesthetized rats. When compared to hippocampal cells, relatively few subicular and entorhinal cells showed a change in mean firing rate following septal inactivation. Entorhinal unit responses to septal inactivation (via tetracaine injection) were also examined in freely moving rats performing a spatial maze task. About one-third of entorhinal cells showed enhanced or reduced firing rates of 40% or more. Also, the spatial distribution of cells found in the superficial, but not deep, entorhinal layers became less clear following septal inactivation. Together, these data are consistent with the hypothesis that manipulation of the medial septum affects hippocampal function via its septosubicular and septo-entorhinal projections in addition to the more direct septohippocampal pathway. Since entorhinal cortical function was affected by tetracaine injection into the septum, it does not appear that direct entorhinal-CA1 afferents were primarily responsible for the maintenance of CA1 location-specific neural activity in previous septal inactivation experiments. Rather, these data are consistent with the hypothesis that the persistence of CA1 place fields was accomplished by intrahippocampal neural network operations.

Computational approaches to hippocampal function

Article

May 1992
CURR OPIN NEUROBIOL

The results of theoretical work have led researchers to suggest that the hippocampal formation may maximize its memory storage capacity by recoding events into patterns that are as dissimilar to one another, and which use as few neurons per event, as possible.

The postsubicular cortex in the rat: characterization of the fourth region of the subicular cortex and its connections

Article

Nov 1990
BRAIN RES

The hippocampal formation contributes importantly to many cognitive functions, and therefore has been a focus of intense anatomical and physiological research. Most of this research has focused on the hippocampus proper and the fascia dentata, and much less attention has been given to the subicular cortex, the origin of most extrinsic projections from the hippocampal formation. The present experiments demonstrate that the postsubiculum is a distinct area of the subicular cortex. The major projections to the postsubiculum originate in the hippocampal formation, the cingulate cortex, and the thalamus (primarily from the anterodorsal (AD) nucleus and to a lesser extent from the anteroventral (AV) and lateral dorsal (LD) nuclei). These projections differ from the thalamic projections to presubiculum and parasubiculum. Efferent projections from the postsubiculum terminate in both cortical and subcortical areas. The cortical projections terminate in the subicular and retrosplenial cortices and in the caudal lateral entorhinal and perirhinal cortices. Subcortical projections primarily end in the AD and the LD nuclei of the thalamus. These thalamic projections end in areas that are distinct from those to which the presubiculum and parasubiculum project. For instance, the postsubiculum has a dense terminal field in the AD nucleus, but presubicular axons terminate predominantly in the AV nucleus. The cortical projections also distinguish postsubiculum. All subicular areas project to the entorhinal cortex, but the postsubicular projection ends in the deep layers (i.e. IV-VI), whereas presubiculum projects to layers I and III, and parasubiculum projects to layer II. Postsubiculum projects to retrosplenial granular b cortex and only incidentally to retrosplenial granular a cortex. In contrast presubiculum projects to the retrosplenial granular a cortex but not to the retrosplenial granular b cortex. These differences clearly mark the postsubiculum, the presubiculum, and the parasubiculum as distinct regions within the subicular cortex and suggest that they subserve different roles in the processing and integration of limbic system information.

Chapter 21 Chapter Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing

Article

Feb 1990
Progr Brain Res

The activity of individual pyramidal cells in the CA1 and CA3 subfields of the rodent hippocampus exhibits a remarkable selectivity for specific locations and orientations of the rat within spatially-extended environments. These cells exhibit high rates of activity when the animal is present within restricted regions of space, referred to as place fields, and are extremely quiet when it is elsewhere. Although this phenomenon has been well studied in the CA fields of the hippocampus, relatively little is known about the spatial and temporal firing characteristics either of the entorhinal cortical inputs to the hippocampus, or of the subicular recipients of the output of hippocampal place cells. We report here on a comparison of spatial and temporal discharge characteristics among entorhinal cortex, CA3 and CA1, and the subiculum. CA3 complex spike cells were significantly more spatially specific than their CA1 counterparts. Neither entorhinal cortex nor subiculum exhibited the highly localized patterns of spatial firing observed in the CA fields. In addition, average discharge rates in these areas were substantially higher. However, particularly in subiculum, there was evidence for spatially consistent, but dispersed, firing in some cells, suggestive of the convergence of a number of CA1 place cells. The patterns observed are not consistent with the hypothesis that spatial selectivity is progressively refined at the various levels of hippocampal processing. Rather, hippocampal output appears to be expressed as a much more highly distributed spatial code than activity within the hippocampus proper. We suggest that the sparse coding used within the hippocampus itself represents a mechanism for increasing the storage capacity of a network whose function is to form associations rapidly.

Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex

Article

Jul 1985

Christer Köhler

The intrahippocampal projections of the subicular complex were studied in the rat with the aid of the anterogradely transported lectin Phaseolus vulgaris leucoagglutinin (PHA‐L). After iontophoretic injections of the lectin into the subiculum proper, presubiculum, or the parasubiculum, axons and terminal processes immunoreactive for PHA‐L were traced to their respective terminal fields within the hippocampal region. After subicular injections PHA‐L‐stained axons could be followed both in a caudal and a rostral direction. The caudally directed fibers course around or within the angular bundle to enter layers VI and V of the medial entorhinal area (MEA). Many fibers penetrate through these layers to terminate in layer IV of the medial and the lateral entorhinal area, which contains a major terminal field of this projection. At more ventral levels, all layers of the entorhinal area are innervated by cells located in the subiculum. Other retrohippocampal projections of the subiculum proper include the deep and the outer two layers of the presubiculum and the medial sector of the parasubiculum, in addition to a massive projection which terminates in the retrosplenial cortex. The rostrally directed projections from the subiculum form a dense innervation of strata lacunosum, radiatum, oriens, and of individual pyramidal cells in the regio superior of the Ammon's horn. All these projections of the subiculum are exclusively ipsilateral. After injections of PHA‐L into layers n and III of the presubiculum, both ipsi‐ and contralateral projections were traced to the outer three layers of the medial entorhinal area; the lateral entorhinal area apparently receives no innervation from the presubiculum. The innervation of layer III is very dense while in layer II and deep layer I, restricted zones of innervation are found. The fibers reach these layers via the deep layers of the MEA and through the molecular layer after first coursing around the parasubiculum. In addition, a minor projection from the presubiculum to the pyramidal cell layer of the subiculum and to the molecular layer of the hippocampal formation was found. PHA‐L injections into the parasubiculum labeled fibers that form a dense innervation of layer II in the MEA and the medial part of the lateral EA, and of the most medial sector of layer III in the MEA. Layer I and the superficial part of layer II of the contralateral MEA also contain a dense terminal network after PHA‐L injections into the parasubiculum. The commissural fibers reach the contralateral side via the dorsal hippocampal commissural system, the angular bundle, and finally through all layers of the contralateral EA. With the exception of a small projection to the molecular layer of the hippocampal formation, the parasubiculum appears not to innervate any of the other hippocampal subfields. Taken together, these studies have shown that each field of the subicular complex has projections restricted to separate layers of the entorhinal area, and thus, that each field participates in its own unique way in the control of entorhinal function.

Hippocampal electrical acitvity and voluntary movement in rat

Article

May 1969
Electroencephalogr Clin Neurophysiol

C.H. Vanderwolf

Stainless steel macro-electrodes were chronically implanted in 24 adult male hooded rats. EEG recordings were taken from the hippocampal formation, diencephalon and neocortex and were correlated with observations of spontaneous or conditioned behavior. Trains of rhythmical 6-12 c/sec waves in the hippocampus and medial thalamus precede and accompany gross voluntary types of movement such as walking, rearing, jumping, etc. Behavioral immobility (in the alert state) and automatic movement patterns such as blinking, scratching, washing the face, licking or biting the fur, chewing food or lapping water are associated with irregular hippocampal activity. Small movements, such as shifts of posture or isolated movements of the head or limbs occurring during immobility, or during grooming or feeding behavior, are associated with rhythmical activity of reduced amplitude and lowered mean frequency. A shock avoidance response is preceded by an increase in wave frequency. Peak frequency is reached just before the occurrence of the motor response. It is suggested that rhythmical slow activity in the hippocampus and diencephalon are the electrical sign of activity in a forebrain mechanism which organizes or initiates higher (voluntary) motor acts. No support is found for previous suggestions that such waves are specifically related to generalized arousal, orienting responses, learning, attention or approach behavior.

Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. Part I. Behavioral correlates and firing repertoires

Article

Dec 1973

James Byrne Ranck, Jr.

Peer Reviewed http://deepblue.lib.umich.edu/bitstream/2027.42/33782/1/0000036.pdf

The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats

Article

Feb 1983

Isolated single units in rat dorsal hippocampus and fascia dentata were classified as 'Theta' or 'Complex-Spike' cells, and their firing characteristics were examined with respect to position, direction and velocity of movement during forced choice, food rewarded search behavior on a radial eight arm maze. Most spikes from CS cells occurred when the animal was located within a particular place on the maze and moving in a particular direction. Theta cells had very low spatial selectivity. Both cell categories had discharge probabilities which increased somewhat as a function of running velocity but tended to asymptote well before half-maximal velocity. The place/direction specificity of CS cells was significantly higher in CA1 than in CA3 and CA3 CS cells exhibited a striking preference for the inward radial direction. The pronounced directional selectivity of CS cells, at least in the present environment, suggests that they fire in response to complex, but specific, stimulus features in the extramaze world rather than to absolute place in a non-egocentric space. An alternative possibility is that the geometrical constraints of the maze surface have a profound influence on the shapes of the response fields of CS cells.

Spatially selective firing properties of hippocampal formation neurons in rodents and primates

Article

Mar 1995
PROG NEUROBIOL

Shane M O'Mara

Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation

Article

Feb 1994

Phase relationship between hippocampal place units and the EEG theta rhythm

Article

Jul 1993

Many complex spike cells in the hippocampus of the freely moving rat have as their primary correlate the animal's location in an environment (place cells). In contrast, the hippocampal electroencephalograph theta pattern of rhythmical waves (7-12 Hz) is better correlated with a class of movements that change the rat's location in an environment. During movement through the place field, the complex spike cells often fire in a bursting pattern with an interburst frequency in the same range as the concurrent electroencephalograph theta. The present study examined the phase of the theta wave at which the place cells fired. It was found that firing consistently began at a particular phase as the rat entered the field but then shifted in a systematic way during traversal of the field, moving progressively forward on each theta cycle. This precession of the phase ranged from 100 degrees to 355 degrees in different cells. The effect appeared to be due to the fact that individual cells had a higher interburst rate than the theta frequency. The phase was highly correlated with spatial location and less well correlated with temporal aspects of behavior, such as the time after place field entry. These results have implications for several aspects of hippocampal function. First, by using the phase relationship as well as the firing rate, place cells can improve the accuracy of place coding. Second, the characteristics of the phase shift constrain the models that define the construction of place fields. Third, the results restrict the temporal and spatial circumstances under which synapses in the hippocampus could be modified.

Jung, M.W. & McNaughton, B.L. Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3, 165-182

Article

Apr 1993

Single neuron activity was recorded in the granular layer of the fascia dentata in freely moving rats, while the animals performed a spatial "working" memory task on an eight-arm maze. Using recording methods that facilitate detection of units with low discharge rates, it was found that the majority (88%) of cells in this layer have mean rates below 0.5 Hz, with a minimum of 0.01 Hz or less. The remaining recorded cells exhibited characteristics typical of the theta interneurons found throughout the hippocampus. Based on several criteria including relative proportion and the relation of their evoked discharges to the population spike elicited by perforant path stimulation, it was concluded that the low-rate cells correspond to granule cells. Granule cells exhibited clear spatially and directionally selective discharge that was at least as selective as that of a sample of CA3 pyramidal cells recorded under the same conditions. Granule cells had significantly smaller place fields than pyramidal cells, and tended to have more discontiguous subfields. There was no spatial correlation among simultaneously recorded adjacent granule cells. Granule cells also exhibited burst discharges reminiscent of complex spikes from pyramidal cells while the animals sat quietly; however, the spike duration of granule cells was significantly shorter than CA3 pyramidal cell spike durations. Under conditions of environmental stability, granule cell place fields were stable for at least several days. Following occasional maze rotations relative to the (somewhat impoverished) visual stimuli of the recording room, granule cell place fields were maintained relative to the distal spatial cues; however, frequent rotations of the maze sometimes resulted in a shift in the reference frame to the maze itself. These observations indicate that granule cells of the fascia dentata provide their CA3 targets with a high degree of spatial information, in the form of a sparsely coded, distributed representation.

IIippocampal formation Characteristics of sparsely encoded associative memory 990) Comparison of spatial and temporal characteristics of neu-ronal activity in sequential stages of hippocampal processing

Jan 1989
443-493451

An~aral Dg
M Witter

An~aral DG, Witter M P (1995) IIippocampal formation. In: '].he rat newous sysrem, second edition (Paxinos G, ed), pp 443-493. San Diego: Academic Press. Aniari S (1989) Characteristics of sparsely encoded associative memory. Neural Ncnvorks 2:451-457. Barnes CA, McNaughton BL, Mizumori SJY, Lonard BW, Lin L-H (1 990) Comparison of spatial and temporal characteristics of neu-ronal activity in sequential stages of hippocampal processing. Prog Brain Rcs 83:287-300.

Neurons of the superficial layer of the lateral entorhinal cortex: Location-specific firing and relations to theta rhythm

Fox SE
Brazhnik E
Muller RU

Jan 1983
41

McNaughton

Jan 1990
407

Rolls

Neurons of the superficial layer of the lateral entorhinal cortex: Location‐specific firing and relations to theta rhythm

Jan 1994
341

Fox SE

Place cells recorded in the parasubiculum of freely moving rats

Abstract

No full-text available

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