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ABSTRACT: Work is reviewed that relates recognition memory to studies of synaptic plasticity mechanisms in perirhinal and prefrontal cortices. The aim is to consider evidence that perirhinal cortex and medial prefrontal cortex store rather than merely transmit information necessary for recognition memory and, if so, to consider what mechanisms are potentially available within these cortices for producing such storage through synaptic change. Interventions with known actions on plasticity mechanisms are reviewed in relation to their effects on recognition memory processes. These interventions importantly include those involving antagonism of glutamatergic and cholinergic receptors but also inhibition of plasticity consolidation and expression mechanisms. It is concluded that there is strong evidence that perirhinal cortex is involved in information storage necessary for object recognition memory and, moreover, that such storage involves synaptic weakening mechanisms including the removal of AMPA glutamate receptors from synapses. There is good evidence that medial prefrontal cortex is necessary for associative and temporal order recognition memory and that this cortex expresses plasticity mechanisms that potentially allow the storage of information. However, the case for medial prefrontal cortex acting as a store requires further support. © 2012 Wiley Periodicals, Inc.
Hippocampus 10/2012; 22(10):2012-31. · 5.18 Impact Factor
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ABSTRACT: Findings of pharmacological studies that have investigated the involvement of specific regions of the brain in recognition memory are reviewed. The particular emphasis of the review concerns what such studies indicate concerning the role of the perirhinal cortex in recognition memory. Most of the studies involve rats and most have investigated recognition memory for objects. Pharmacological studies provide a large body of evidence supporting the essential role of the perirhinal cortex in the acquisition, consolidation and retrieval of object recognition memory. Such studies provide increasingly detailed evidence concerning both the neurotransmitter systems and the underlying intracellular mechanisms involved in recognition memory processes. They have provided evidence in support of synaptic weakening as a major synaptic plastic process within perirhinal cortex underlying object recognition memory. They have also supplied confirmatory evidence that that there is more than one synaptic plastic process involved. The demonstrated necessity to long-term recognition memory of intracellular signalling mechanisms related to synaptic modification within perirhinal cortex establishes a central role for the region in the information storage underlying such memory. Perirhinal cortex is thereby established as an information storage site rather than solely a processing station. Pharmacological studies have also supplied new evidence concerning the detailed roles of other regions, including the hippocampus and the medial prefrontal cortex in different types of recognition memory tasks that include a spatial or temporal component. In so doing, they have also further defined the contribution of perirhinal cortex to such tasks. To date it appears that the contribution of perirhinal cortex to associative and temporal order memory reflects that in simple object recognition memory, namely that perirhinal cortex provides information concerning objects and their prior occurrence (novelty/familiarity).
Neuropsychologia 07/2012; · 3.64 Impact Factor
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ABSTRACT: The aim was to investigate the role of calcium-calmodulin-dependent protein kinase (CAMK)II in object recognition memory. The performance of rats in a preferential object recognition test was examined after local infusion of the CAMKII inhibitors KN-62 or autocamtide-2-related inhibitory peptide (AIP) into the perirhinal cortex. KN-62 or AIP infused after acquisition impaired memory tested at 24 h, indicating an involvement of CAMKII in the consolidation of recognition memory. Memory was impaired when KN-62 was infused at 20 min after acquisition or when AIP was infused at 20, 40, 60 or 100 min after acquisition. The time-course of CAMKII activation in rats was further examined by immunohistochemical staining for phospho-CAMKII(Thre286)alpha at 10, 40, 70 and 100 min following the viewing of novel and familiar images. At 70 min, processing novel images resulted in more phospho-CAMKII(Thre286)alpha-stained neurons in the perirhinal cortex than did the processing of familiar images, consistent with the viewing of novel images increasing the activity of CAMKII at this time. This difference was eliminated by prior infusion of AIP. These findings establish that CAMKII is active within the perirhinal region between approximately 20 and 100 min following learning and then returns to baseline. Thus, increased CAMKII activity is essential for the consolidation of long-term object recognition memory but continuation of that increased activity throughout the 24 h memory delay is not necessary for maintenance of the memory.
European Journal of Neuroscience 10/2009; 30(6):1128-39. · 3.63 Impact Factor
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ABSTRACT: To investigate neuronal processing during monkeys' performance of a visual conditional discrimination task, recordings were made from four areas of prefrontal cortex (ventromedial, orbitofrontal, dorsolateral and anterior cingulate) where lesions have been shown to produce impairment of such tasks. Of 1911 recorded neurons, 573 (31%) responded to elements of the task. This proportion was less than the 50% previously reported as responsive in temporal cortex under the same conditions, suggesting sparser encoding in prefrontal than temporal cortex. Of the responsive prefrontal neurons, 165 (29%) responded differently on the different types of trial, so signalling various types of information relevant to task performance and cognition. In line with recent lesion findings, in the dorsolateral region the incidence of such differentially responsive neurons was only an eighth that in the other regions. The relatively high incidence of neuronal responses that encoded a potential instruction cue rather than specific individual stimulus arrangements was consistent with the animals solving the task by using such information, though other neuronal responses could have enabled the task to have been solved by rote learning. Compared to temporal neurons, prefrontal responses more frequently coded information relating to the planned behavioural response rather than perceptual aspects of the task. Population differential response latencies were long (> approximately 225 ms) in prefrontal cortex. A comparison of such differential latencies between temporal and prefrontal cortex indicated that potential information flow was likely to be primarily from temporal to prefrontal cortex rather than vice versa.
European Journal of Neuroscience 05/2007; 25(9):2916-26. · 3.63 Impact Factor
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ABSTRACT: Activity of the immediate early genes c-fos and zif268 was compared across hemispheres in rats with unilateral, excitotoxic lesions of the hippocampus (dentate gyrus and CA fields 1-4). Counts of the protein products of these genes were made shortly after rats performed a test of spatial working memory in the radial-arm maze, a task that is sensitive to bilateral lesions of the hippocampus. Unilateral hippocampal lesions produced evidence of widespread hypoactivity. Significant reductions in immediate early gene counts were observed within all three anterior thalamic nuclei, as well as the entorhinal, perirhinal, and postrhinal cortices, and much of the subicular complex. In contrast, no observable changes were detected in the anterior cingulate, infralimbic or prelimbic cortices, as well as several amygdala nuclei, even though many of these regions receive projections from the subiculum. Instead, the immediate early gene changes were closely linked to sites that are thought to be required for successful task performance, with both immediate early genes giving similar patterns of results. The findings support the notion that the anterior thalamic nuclei, hippocampus, and parahippocampal cortices form the key components of an interdependent neuronal network involved in spatial mnemonic processing.
Neuroscience 03/2006; 137(3):747-59. · 3.38 Impact Factor
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ABSTRACT: Benzodiazepines, including lorazepam, are widely used in human medicine as anxiolytics or sedatives, and at higher doses can produce amnesia. Here we demonstrate that in rats lorazepam impairs both recognition memory and synaptic plastic processes (long-term depression and long-term potentiation). Both impairments are produced by actions in perirhinal cortex. The findings thus establish a mechanism by means of which benzodiazepines impair recognition memory. The findings also strengthen the hypotheses that the familiarity discrimination component of recognition memory is dependent on reductions in perirhinal neuronal responses when stimuli are repeated and that these response reductions are due to a plastic mechanism also used in long-term depression.
European Journal of Neuroscience 11/2004; 20(8):2214-24. · 3.63 Impact Factor
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ABSTRACT: The novelty of a cue may arise from the presence of an element that has not previously been experienced or from familiar elements that have been rearranged. The present study mapped the anatomical basis of responding to this second form of novelty. For this, rats were trained on a working memory spatial task in a radial-arm maze in a cue-controlled environment. On the final test day the positions of the familiar, extra-maze cues were rearranged for half of the rats (group Novel). The spatial configuration of the cues now matched that of the control rats (group Familiar). Neuronal activation, as measured by the immediate early gene, c-fos, was then compared between the two groups. Rearrangement of visual stimuli led to significant increases in Fos-positive cells in various hippocampal subfields (rostral CA1, rostral CA3 and rostral dentate gyrus) as well as the parietal cortex and the postsubiculum. In contrast, no changes were observed in other sites including the perirhinal cortex, postrhinal cortex, lateral and medial entorhinal cortices, retrosplenial cortices, or anterior thalamic nuclei. These results highlight the selective involvement of the hippocampus for processing novel rearrangements of visual stimuli and suggest that this involvement is intrinsic as it is independent of the parahippocampal cortices. This pattern of Fos changes is the mirror image of that repeatedly found for novel individual stimuli (perirhinal increase, no hippocampal change), demonstrating that these two forms of novelty have qualitatively different neural attributes.
Neuroscience 02/2004; 124(1):43-52. · 3.38 Impact Factor
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ABSTRACT: It has previously been shown that the neuropeptide galanin plays a role in the age-dependent regulation of hippocampal synaptic plasticity and spatial memory. Here, we further extend these studies by demonstrating that galanin knockout mice also have deficits in an object-in-place spatial memory task. In contrast however, there is no deficit in single item object recognition memory, a memory that depends on perirhinal cortex. Furthermore, in perirhinal cortex slices there are no differences in activity-dependent long-term potentiation or depotentiation, nor in muscarinic receptor-dependent long-term depression between galanin knockout mice and wild-type litter-mates. Therefore, these results suggest that galanin has a differential role in hippocampal-dependent and perirhinal cortex-dependent memory.
Neuropharmacology 02/2003; 44(1):40-8. · 4.81 Impact Factor
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ABSTRACT: Many studies indicate that recognition memory involves at least two separable processes, familiarity discrimination and recollection. Aspects of what is known of potential neuronal substrates of familiarity discrimination are reviewed. Lesion studies have established that familiarity discrimination for individual visual stimuli is effected by a system centred on the perirhinal cortex of the temporal lobe. The fundamental change that encodes prior occurrence of such stimuli appears to be a reduction in the response of neurons in anterior inferior temporal (including perirhinal) cortex when a stimulus is repeated. The neuronal responses rapidly signal the presence of a novel stimulus, and are evidence of long-lasting learning after a single exposure. Computational modelling indicates that a neuronal network based on such a change in responsiveness is potentially highly efficient in information theoretic terms. Processes that occur in long-term depression within the perirhinal cortex provide candidate synaptic plastic mechanisms for that underlying the change, but such linkage remains to be experimentally established.
Philosophical Transactions of The Royal Society B Biological Sciences 09/2002; 357(1424):1083-95. · 6.40 Impact Factor
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ABSTRACT: In this study we have investigated mechanisms underlying enhancement by group II metabotropic glutamate (mGlu) receptors of group I mGlu receptor-induced calcium mobilization. Inhibition of protein kinase A (PKA) caused an enhancement of mGlu5 receptor-mediated calcium mobilization and occluded the enhancement by group II mGlu receptors. A peptide (Ht31) that prevents interaction between A-kinase anchoring protein (AKAP) and PKA also enhanced mGlu5-mediated calcium mobilization. Enhancement of mGlu5 function, by inhibition of PKA or by activation of group II mGlu receptors, was prevented by the protein phosphatase 2B (PP2B) inhibitor cyclosporin A. Furthermore, the enhancement by activation of group II mGlu receptors was prevented by raising intracellular cAMP. These results suggest that the regulation by PKA and PP2B of phosphorylation of a substrate on mGlu5 and/or on group II mGlu receptors is intimately involved in the mechanisms underlying interaction between group II mGlu and mGlu5 receptors. Long-term depression (LTD) in perirhinal cortex requires group I, group II and NMDA receptor activation at resting membrane potentials but does not require group II mGlu receptor activation at depolarized potentials. We previously suggested that interaction between group I and group II mGlu receptors is required for induction of LTD at resting potentials. In support of this, we demonstrate in perirhinal cortex slices that blocking mechanisms underlying mGlu receptor synergy (by raising intracellular cAMP or by inhibition of PP2B) selectively prevented LTD at resting membrane potentials. This study thus provides a potential explanation for the co-requirement in LTD of group I and group II mGlu receptor activation. Similar mechanisms of synergistic interaction may also be important in other physiological processes dependent on mGlu receptors.
The Journal of Physiology 06/2002; 540(Pt 3):895-906. · 4.72 Impact Factor
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ABSTRACT: To provide information about the possible regions involved in auditory recognition memory, this study employed an imaging technique that has proved valuable in the study of visual recognition memory. The technique was used to image populations of neurons that are differentially activated by novel and familiar auditory stimuli, thereby paralleling previous studies of visual familiarity discrimination. Differences evoked by novel and familiar sounds in the activation of neurons were measured in different parts of the rat auditory pathway by immunohistochemistry for the protein product (Fos) of the immediate early gene c-fos. Significantly higher counts of stained neuronal nuclei (266 +/- 21/mm2) were evoked by novel than by familiar sounds (192 +/- 17/mm2) in the auditory association cortex (area Te3; AudA). No such significant differences were found for the inferior colliculus, primary auditory cortex, postrhinal cortex, perirhinal cortex (PRH), entorhinal cortex, amygdala or hippocampus. These findings are discussed in relation to the results of lesion studies and what is known of areas involved in familiarity discrimination for visual stimuli. Differential activation is produced by novel and familiar individual stimuli in sensory association cortex for both auditory and visual stimuli, whereas the PRH is differentially activated by visual but not auditory stimuli. It is suggested that this latter difference is related to the nature of the particular auditory and visual stimuli used.
European Journal of Neuroscience 08/2001; 14(1):118-24. · 3.63 Impact Factor
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ABSTRACT: There is strong evidence that decrements in neuronal activation in perirhinal cortex when a novel stimulus is repeated provide a neural substrate of visual recognition memory. There is also strong evidence that muscarinic acetylcholine (ACh) receptors are involved in learning and memory. However, the mechanisms underlying neuronal decrements in the perirhinal cortex and the basis of ACh involvement in learning and memory are not understood. In an in vitro preparation of rat perirhinal cortex we now demonstrate that activation of ACh receptors by carbachol (CCh) produces long-lasting depression (LLD) of synaptic transmission that is dependent on muscarinic M1 receptor activation. Crucially, the induction of this form of LLD requires neither N-methyl-D-aspartate receptor activation nor synaptic stimulation. CCh-induced LLD was not blocked by the protein kinase C inhibitors staurosporine or BIM, or by the protein phosphatase inhibitor okadaic acid. However, each of cyclopiazonic acid (an agent that depletes intracellular calcium stores) and anisomycin (an inhibitor of protein synthesis) significantly reduced the magnitude of CCh-induced LLD. These mechanisms triggered by muscarinic receptor activation could play a role in the induction and/or expression of certain forms of activity-dependent long-term depression in perirhinal cortex. An understanding of CCh-induced LLD may thus provide clues to the mechanisms underlying lasting neuronal decrements that occur in the perirhinal cortex and hence for neural substrates of visual recognition memory.
European Journal of Neuroscience 08/2001; 14(1):145-52. · 3.63 Impact Factor
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ABSTRACT: There is strong converging evidence that the intermediate and medial part of the hyperstriatum ventrale of the chick brain is a memory store for information acquired through the learning process of imprinting. Neurons in this memory system come, through imprinting, to respond selectively to the imprinting stimulus (IS) neurons and so possess the properties of a memory trace. Therefore, the responses of the intermediate and medial part of the hyperstriatum ventrale neurons to a visual imprinting stimulus were determined before, during, and after training. Of the total recorded population, the proportions of IS neurons shortly after each of two 1-h training sessions were significantly higher (approximately 2 times) than the pretraining proportion. However, approximately 4.5 h later this proportion had fallen significantly and did not differ significantly from the pretraining proportion. Nevertheless, approximately 21.5 h after the end of training, the proportion of IS neurons was at its highest (approximately 3 times the pretraining level). No significant fluctuations occurred in the proportions of neurons responding to the alternative stimulus. In addition, nonmonotonic changes were found commonly in the activity of 230 of the neurons tracked individually from before training to shortly after the end of training. Thus the pattern of change in responsiveness both at the population level and at the level of individual neurons was highly nonmonotonic. Such a pattern of change is not consistent with simple models of memory based on synaptic strengthening to asymptote. A model is proposed that accounts for the changes in the population responses to the imprinting stimulus in terms of changes in the responses of individual neurons.
Proceedings of the National Academy of Sciences 05/2001; 98(9):5282-7. · 9.68 Impact Factor
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ABSTRACT: 1. We have investigated the prediction of a relationship between the magnitude of activity-dependent increases in postsynaptic calcium and both the magnitude and direction of synaptic plastic change in the central nervous system. 2. Activity-dependent increases in calcium were buffered to differing degrees using a range of concentrations of EGTA and the effects on synaptic plasticity were assessed. Activity-dependent synaptic plasticity was induced during whole-cell recording in rat perirhinal cortex in vitro. In control conditions (0.5 mM EGTA) low frequency stimulation (LFS; 200 stimuli) delivered to neurones held at -40 or -70 mV induced long-term depression (LTD) or, at -10 mV, induced long-term potentiation (LTP). 3. The relationship between EGTA concentration (0.2 to 10 mM) and the magnitude of LTD was examined. This relationship described a U-shaped curve, as predicted by models of synaptic plasticity. This provides strong evidence that the magnitude of LTD is determined by the magnitude of the increase in intracellular calcium concentration. 4. LFS paired with depolarisation to -10 mV induced LTD, no change or LTP as activity-dependent postsynaptic calcium levels were allowed to increase progressively by the use of progressively lower concentrations of buffer (10 to 0.2 mM EGTA). 5. We investigated if the lack of plasticity that occurs at the transition between LTD and LTP is due to induction of both of these processes with zero net change, or is due to neither LTD nor LTP being induced. These experiments were possible as LTP but not LTD was blocked by the protein kinase inhibitor staurosporine while LTD but not LTP was blocked by the mGlu receptor antagonist MCPG. At the transition between LTD and LTP, blocking LTP mechanisms did not uncover LTD whilst blocking LTD mechanisms did not uncover LTP. This suggests that the transition between LTD and LTP is due to the lack of induction of both of these processes and also suggests that these two processes are induced independently of one another.
The Journal of Physiology 05/2001; 532(Pt 2):459-66. · 4.72 Impact Factor
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ABSTRACT: The hallmark of medial temporal lobe amnesia is a loss of episodic memory such that patients fail to remember new events that are set in an autobiographical context (an episode). A further symptom is a loss of recognition memory. The relationship between these two features has recently become contentious. Here, we focus on the central issue in this dispute--the relative contributions of the hippocampus and the perirhinal cortex to recognition memory. A resolution is vital not only for uncovering the neural substrates of these key aspects of memory, but also for understanding the processes disrupted in medial temporal lobe amnesia and the validity of animal models of this syndrome.
Nature reviews. Neuroscience 02/2001; 2(1):51-61. · 30.44 Impact Factor
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European Journal of Neuroscience. 01/2001; 14:145-52.
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ABSTRACT: Activity of the immediate early gene c-fos was compared across hemispheres in rats with unilateral fornix lesions. To engage Fos production, rats first performed a radial arm maze task that is severely disrupted by bilateral fornix lesions. Using immunohistochemical techniques, Fos-positive cells were visualized and counted in 39 sites in both hemispheres. Fornix lesions led to a significant reduction in Fos in all ipsilateral hippocampal subfields, as well as the entorhinal cortex and most of the subicular complex. Other sites that showed reduced activity included the ipsilateral retrosplenial, anterior cingulate, and postrhinal cortices. Subcortical regions showing significant Fos decreases included the anterior thalamic nuclei, supramammillary nucleus, diagonal band of Broca, and lateral septum. Thus, the effects of fornix lesions extended beyond the hippocampal formation and included sites not directly innervated by the tract. These changes were nevertheless selective, as shown by the lack of hemispheric difference in any of the preselected control sites, the perirhinal cortex, or nucleus accumbens. Furthermore, there were no hemispheric differences in an additional group of animals with unilateral fornix lesions that were killed directly from the home cage. The location of Fos changes closely corresponded to those brain regions that when lesioned disrupt spatial working memory. Moreover, there was a correspondence between those brain regions that show increased Fos production in normal animals performing the radial arm maze task and those affected by fornix lesions. These results show that fornix transection has widespread, but selective, effects on a network of structures normally activated by spatial memory processes, with these effects extending beyond the hippocampal formation.
Journal of Neuroscience 12/2000; 20(21):8144-52. · 7.11 Impact Factor
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ABSTRACT: We compared neuronal activation, as measured by Fos staining, during different spatial tasks in two experiments. The counts of Fos-stained neurons in the hippocampus increased as the spatial demands of the tasks increased, the tasks having been carefully matched for other factors. In Experiment 1, matched groups of rats either ran a standard eight-arm radial maze task or were trained to run up and down just one arm of the maze; the number of runs and rewards was identical in both conditions. In Experiment 2, rats were trained on the eight-arm maze but in different rooms. On the critical test day, both groups were run in the same room so that one group now performed with novel landmarks. All hippocampal subfields (dentate gyrus, CA3, CA1, dorsal, ventral, and caudal subiculum) showed a relative increases in c-fos activation in the eight-arm (Experiment 1) and novel room (Experiment 2) conditions, the sole exception being the ventral subiculum in Experiment 2. Although increased c-fos activation was found in both dorsal and ventral hippocampus, in Experiment 2 the relative increase was significantly greater in the dorsal hippocampus. Parahippocampal cortices responded heterogeneously: the perirhinal cortex failed to show increased activation in both experiments, in contrast to the entorhinal and postrhinal cortices. Subsequent comparisons confirmed that the perirhinal and postrhinal cortices responded in qualitatively different ways, the perirhinal cortex differing from the rest of the hippocampal formation. These experiments, which provide the first analysis of hippocampal Fos production during tests of allocentric spatial working memory, reveal that all components of the hippocampus are activated, but that under certain conditions the dorsal hippocampus is disproportionately involved.
Journal of Neuroscience 05/2000; 20(7):2711-8. · 7.11 Impact Factor
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ABSTRACT: Excitatory synaptic transmission in the perirhinal cortex exhibits marked homosynaptic paired pulse depression (PPD) at inter-pulse intervals between 100 and 1000 ms, being maximal at 200 ms. Additionally, there is greater PPD with stimulation of the pathway from the temporal cortex side than with stimulation of the pathway from the entorhinal cortex side. We establish that this frequency-dependent depression relies on the activation of GABAB (gamma-aminobutyric acid) receptors. PPD in both temporal and entorhinal pathways is abolished by either of the selective GABAB receptor antagonists, 3-N[1-(S)-(3, 4-dichlorophenyl)ethyl]amino-2-(S)-hydroxypropyl-p-benzyl-phosphinic acid (CGP55845A) or 3-amino-propyl(diethoxymethyl)phosphinic acid (CGP35348). Barium which blocks G-protein-coupled, inwardly rectifying potassium channels, does not block PPD. Heterosynaptic depression mediated by GABAB receptors was also observed. The depression of the entorhinal pathway by stimulation of the temporal pathway is greater than depression of the temporal pathway by stimulation of the entorhinal pathway. Moreover, PPD increases with stimulus strength and the depression is enhanced by short trains of stimuli, consistent with stronger stimulation resulting in more GABA reaching GABAB receptors on excitatory glutamatergic synapses. Synaptic activation of GABAB receptors may be important in regulating excitability in a frequency-dependent manner with maximal depression occurring at approximately 5 Hz, which approximates to the theta rhythm. That homosynaptic and heterosynaptic depression by stimulation of the temporal pathway is greater than by stimulation of the entorhinal pathway suggests that activation of temporal feedforward connections to the perirhinal cortex can dominate the GABAergic control of synaptic activity within the perirhinal cortex.
European Journal of Neuroscience 04/2000; 12(3):803-9. · 3.63 Impact Factor
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ABSTRACT: We demonstrate a form of long-term depression (LTD) in the perirhinal cortex that relies on interaction between different glutamate receptors. Group II metabotropic glutamate (mGlu) receptors facilitated group I mGlu receptor-mediated increases in intracellular calcium. This facilitation plus NMDA receptor activation may be necessary for induction of LTD at resting membrane potentials. However, depolarization enhanced NMDA receptor function and removed the requirement of synergy between group I and group II mGlu receptors: under these conditions, activation of only NMDA and group I mGlu receptors was required for LTD. Such glutamate receptor interactions potentially provide new rules for synaptic plasticity. These forms of LTD occur in the perirhinal cortex, where long-term decreases in neuronal responsiveness may mediate recognition memory.
Nature Neuroscience 03/2000; 3(2):150-6. · 15.53 Impact Factor
