Presubicular and parasubicular cortical neurons of the rat: Electrophysiological and morphological properties

Department of Physiology, State University of New York Health Science Center at Brooklyn 11203, USA.
Hippocampus (Impact Factor: 4.16). 01/1997; 7(2):117-29. DOI: 10.1002/(SICI)1098-1063(1997)7:2<117::AID-HIPO1>3.0.CO;2-K
Source: PubMed


Intracellular recordings and Neurobiotin-injection were used to examine the electrophysiology and morphology of presubicular and parasubicular cortical neurons in horizontal slices from rat brains. Evoked responses were obtained by stimulation of subicular and entorhinal cortices. Stellate cells were recorded in layers II and V of presubiculum and parasubiculum. Superficial layer cells had spiny dendrites that were found to reach layer I. Deep layer cells had sparsely spiny dendrites or dendrites without spines that did not reach past layer IV. Pyramidal cells were recorded in layers III and V of presubiculum and layers II and V of parasubiculum. Superficial layer cells had spiny dendrites that were found to reach layer I. Deep layer cells had sparsely spiny dendrites or dendrites without spines that could reach layer II. Electrophysiologically, stellate and pyramidal cells were similar to one another, regardless of cell layer, exhibiting repetitive single spiking in response to depolarizing current injection. No cells were found to burst in response to current injection. While there were subtle electrophysiological differences among the cell types, stellate cells were more similar to pyramidal cells from the same or adjacent layers than to other stellate cells from more distant layers. Similarly, pyramidal cells were electrophysiologically more similar to nearby stellate cells than to other distant pyramidal cells. Cells of all layers responded to subicular stimulation with a short latency (< 9 ms), excitatory postsynaptic potential. Superficial layer cells responded at short (< 9 ms), longer (10-20 ms) and very long latencies (> 20 ms) to stimulation of superficial layers of medial entorhinal cortex. Deep layer cells responded at short latencies (< 9 ms) to stimulation of deep layers of medial entorhinal cortex. Many cells responded to both subicular and entorhinal inputs. Both pyramidal and stellate cells in the deep layer of pre/parasubiculum could exhibit population bursting behavior in response to stimulation of subiculum or entorhinal cortex. The results define the cellular morphology and basic electrophysiology of presubicular and parasubicular neurons of the rat brain as a step toward understanding the physiology of the retrohippocampal cortices.

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    • "Single-cell patch-clamp recordings were performed from the subiculum, presubiculum and medial EC, layer V. Previously published works describing the anatomical location and electrophysiological characteristics of cells from these regions were used to ensure that the studied cells were assigned to the correct region (Funahashi and Stewart, 1997; Menendez de la Prida et al., 2003; Canto and Witter, 2012). For the characterization of cellular discharge and membrane properties, hyper-and depolarizing current steps were applied (in 50-pA steps of 500-ms duration, starting from À250 pA) in current clamp mode. "
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    ABSTRACT: Norepinephrine acting via β-adrenergic receptors (β-AR) plays an important role in hippocampal plasticity including the subiculum which is the principal target of CA1 pyramidal cells and which controls information transfer from the hippocampus to other brain regions including the neighboring presubiculum and the entorhinal cortex (EC). Subicular pyramidal cells are classified as regular- and burst-spiking cells. Activation of β-ARs at CA1-subiculum synapses induces long-term potentiation (LTP) in burst- but not in regular-spiking cells (Wojtowicz et al., 2010). To elucidate seizure-associated disturbances in the norepinephrine-dependent modulation of hippocampal output, we investigated the functional consequences of the β-AR-dependent synaptic plasticity at CA1-subiculum synapses for the transfer of hippocampal output to the parahippocampal region in the pilocarpine model of temporal lobe epilepsy. Using single-cell and multi-channel field recordings in slices, we studied β-AR-mediated changes in the functional connectivity between CA1, the subiculum and its target-structures. We confirm that application of the β-adrenergic agonist isoproterenol induces LTP in subicular burst- but not regular-spiking cells. Due to the distinct spatial distribution of regular- and burst-spiking cells in the proximo-to-distal axis of the subiculum, in field recordings, LTP was significantly stronger in the distal than in the proximal subiculum. In pilocarpine-treated animals, β-AR-mediated LTP was strongly reduced in the distal subiculum. The attenuated LTP was associated with a disturbed polysynaptic transmission from the CA1, via the subiculum to the presubiculum, but with a preserved transmission to the medial EC. Our findings suggest that synaptic plasticity may influence target related information flow and that such regulation is disturbed in pilocarpine-treated epileptic rats. Copyright © 2014. Published by Elsevier Ltd.
    Full-text · Article · Dec 2014 · Neuroscience
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    • "We used electrophysiological parameters and unsupervised hierarchical cluster analysis to classify cell types in PrS, similar to our recent classification of cells in deep layers of the MEA (Pilli et al., 2012). LII and LIII of PrS are typically described as a combined structure in the literature (superficial layers of PrS) and have been described as containing a functionally homogeneous cell population possessing afferent projections that show great overlap (Funahashi and Stewart, 1997a; Honda and Ishizuka, 2004; Menendez de la Prida et al., 2003; Simonnet et al., 2013). Our study shows that both LII and LIII contain a physiologically diverse population of cell types with distinct laminar distributions, patterns of projection, and functional attributes. "
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    ABSTRACT: The presubiculum (PrS) plays critical roles in spatial information processing and memory consolidation and has also been implicated in temporal lobe epileptogenesis. Despite its involvement in these processes, a basic structure-function analysis of PrS cells remains far from complete. To this end, we performed whole-cell recording and biocytin-labeling of PrS neurons in layer (L) II and LIII to examine their electrophysiological and morphological properties. We characterized the cell types based on electrophysiological criteria, correlated their gross morphology, and classified them into distinct categories using unsupervised hierarchical cluster analysis. We identified seven distinct cell types: regular-spiking (RS), irregular-spiking (IR), initially-bursting (IB), stuttering (Stu), single-spiking (SS), fast-adapting (FA), and late-spiking (LS) cells, of which RS and IB cells were common to LII and LIII, LS cells were specific to LIII, and the remaining cell types were identified exclusively in LII. Recorded neurons were either pyramidal or non-pyramidal shaped, and barring Stu cells, displayed spine-rich dendrites. The RS, IB and IR cells appeared to be projection neurons based on extension of their axons into LIII of the medial entorhinal area (MEA) and/or angular bundle. We conclude that layers II and III of PrS are distinct in their neuronal populations and together constitute a more diverse population of neurons than previously suggested. PrS neurons serve as major drivers of circuits in superficial (LII-III) entorhinal cortex (ERC) and couple neighboring structures through robust afferentation thereby substantiating presubiculum's critical role in the parahippocampal region. J. Comp. Neurol., 2013. © 2013 Wiley Periodicals, Inc.
    Full-text · Article · Sep 2013 · The Journal of Comparative Neurology
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    • "Stellate cells had 3 to 5 basal dendrites emanating from the soma that bifurcated several times in a pattern restricted to the superficial layers (Fig. 1A1). Stellate cells typically had spiny dendrites throughout all processes [23]. Pyramidal cells typically had multiple basal dendrites that occasionally extended to the border between layer IIIs and IV and one or two apical dendrites that extended to layer I (Fig. 1A2). "
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    ABSTRACT: The parasubiculum (PaS) is a component of the hippocampal formation that sends its major output to layer II of the entorhinal cortex. The PaS receives strong cholinergic innervation from the basal forebrain that is likely to modulate neuronal excitability and contribute to theta-frequency network activity. The present study used whole cell current- and voltage-clamp recordings to determine the effects of cholinergic receptor activation on layer II PaS neurons. Bath application of carbachol (CCh; 10-50 µM) resulted in a dose-dependent depolarization of morphologically-identified layer II stellate and pyramidal cells that was not prevented by blockade of excitatory and inhibitory synaptic inputs. Bath application of the M1 receptor antagonist pirenzepine (1 µM), but not the M2-preferring antagonist methoctramine (1 µM), blocked the depolarization, suggesting that it is dependent on M1 receptors. Voltage-clamp experiments using ramped voltage commands showed that CCh resulted in the gradual development of an inward current that was partially blocked by concurrent application of the selective Kv7.2/3 channel antagonist XE-991, which inhibits the muscarine-dependent K(+) current I M. The remaining inward current also reversed near EK and was inhibited by the K(+) channel blocker Ba(2+), suggesting that M1 receptor activation attenuates both I M as well as an additional K(+) current. The additional K(+) current showed rectification at depolarized voltages, similar to K(+) conductances mediated by Kir 2.3 channels. The cholinergic depolarization of layer II PaS neurons therefore appears to occur through M1-mediated effects on I M as well as an additional K(+) conductance.
    Full-text · Article · Mar 2013 · PLoS ONE
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