Distinct Ensemble Codes in Hippocampal Areas CA3 and CA1

Leutgeb, Stefan; Leutgeb, Jill K.; Treves, Alessandro; Moser, May‐Britt; Moser, Edvard I

doi:10.1126/science.1100265

Cited by 709 publications

(780 citation statements)

References 32 publications

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“…Place fields in CA1 and CA3 are slightly less spatially tuned and considerably less stable in novel versus familiar environments [74]; this may indicate that CA1 activity is dominated by direct, rapid, but unprocessed EC-CA2 input under these conditions, whereas slow refinement of CA1 spatial coding over days [75] relies on CA3-DG-CA1 processing; some lesion data are consistent with this. For example, knife cuts between CA3 and CA1 did not impair rats in a spatial learning task and resulted in CA1 place fields only slightly larger than those of the control rats [76].…”

Section: Selecting Circuits Within Circuits: Who Does What When?supporting

confidence: 72%

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Updating hippocampal representations: CA2 joins the circuit

Jones

McHugh

2011

Trends in Neurosciences

114

106

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The hippocampus integrates the encoding, storage and recall of memories, binding the spatiotemporal and sensory information that constitutes experience and keeping episodes in their correct context. The rapid and accurate processing of such daunting volumes of continuouslychanging data relies on dynamically assigning different aspects of mnemonic processing to specialized, interconnected networks corresponding to the anatomical subfields of dentate gyrus (DG), CA3 and CA1. However, differentially processed information ultimately has to be reintegrated into conjunctive representations, and this is unlikely to be achieved by unidirectional, sequential steps through a DG-CA3-CA1 loop. In this Review, we highlight recently discovered anatomical and physiological features that are likely to necessitate updates to the hippocampal circuit diagram, particularly by incorporating the oft-neglected CA2 region.3

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Section: Selecting Circuits Within Circuits: Who Does What When?supporting

confidence: 72%

“…The hippocampus is typically taken as a model of sequential processing in the nervous system, [74]) via activation of the recurrent network. Inhibition in the DG dominates and helps to ensure a unique and sparse ensemble is activated.…”

Section: Discussionmentioning

confidence: 99%

Updating hippocampal representations: CA2 joins the circuit

Jones

McHugh

2011

Trends in Neurosciences

114

106

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“…It is tempting, however, to relate these results to recent evidence indicating that the CA3 field exhibits more abrupt activity changes in response to changes in stimulus input than does CA1 -a distinction that is believed to correspond to the theoretical constructs of pattern separation versus completion, respectively (Bakker et al, 2008;Leutgeb et al, 2004;Vazdarjanova & Guzowski, 2004). From this perspective, the present findings reflect the tendency of CA3 to categorize input (in this case, new versus old items) in an 'all or none' fashion, while CA1 demonstrates a more continuous (less differentiated) response to the same change in input (Bakker et al, 2008).…”

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confidence: 89%

Multiple repetitions reveal functionally and anatomically distinct patterns of hippocampal activity during continuous recognition memory

2008

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We used a continuous recognition procedure that included multiple presentations of test items, along with high-resolution functional magnetic resonance imaging (fMRI), to investigate the relationship between item novelty and recognition-related activity in the medial temporal lobe (MTL). In several regions of hippocampus and parahippocampal cortex, activity elicited by new items exceeded that for old items, whereas no MTL regions exhibited greater activity for old items. Critically, anatomically-distinct regions of MTL were engaged by item novelty in two different ways, as evidenced by statistically-dissociable profiles of activity. In bilateral medial hippocampus and left posterior parahippocampal cortex, activity followed a categorical profile in which it was greater for new than old items but did not differ further with additional presentations of old items. By contrast, effects in adjacent regions of right lateral hippocampus and left parahippocampal cortex were graded, whereby activity declined linearly with respect to each successive item presentation. These findings suggest that the relationship between hippocampal (and parahippocampal) activity and continuous psychological dimensions, such as item novelty, cannot be captured by a unitary function. Keywords novelty; familiarity; hippocampus; fMRI; high-resolution Consistent with human and animal lesion data implicating MTL in recognition memory (for reviews, see Brown & Aggleton, 2001;Eichenbaum et al., 2007;Squire et al., 2007), fMRI and intracranial (local field potential and single-neuron) recording studies have demonstrated that hippocampal activity is modulated by the study status of recognition test items (e.g., Grunwald et al., 1998;Heit et al., 1988; for a review of fMRI findings, see Henson, 2005). Among event-related fMRI studies employing separate study and test phases, it has occasionally been reported that correctly-recognized (old) items elicit greater hippocampal activity than correctly-rejected (new) items (e.g., Donaldson et al., 2001;Stark & Squire, 2001). More frequently, enhanced hippocampal activity has been reported for recognition test items that are accompanied by either "remember" or accurate source memory judgments, relative to when items are designated with "know" responses or lack source information (e.g., Cansino et al., 2002;Eldridge et al., 2000;Johnson & Rugg, 2007;Wheeler & Buckner, 2004;Woodruff et al., 2005;Yonelinas et al., 2005 to imply that enhanced hippocampal activity is associated with the retrieval (recollection) of qualitative information about a study episode, rather than an acontextual sense of familiarity (Rugg & Yonelinas, 2003; but see Squire et al., 2007). Of significance, however, is that other fMRI studies of recognition memory have reported greater hippocampal activity for new compared to old items (e.g., Duzel et al., 2003;Rombouts et al., 2001;. Such findings have been interpreted as evidence that the hippocampus is sensitive to stimulus novelty, with elevated activity reflecting an allocation ...

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“…There are many reports of place fields that rapidly reorganize (i.e., change field location and/or firing rate) when the environment changes, while other place fields persist despite changes in contextual features Lee et al, 2004;Leutgeb et al, 2004). The responsive place fields may reflect the current contextual features while the persistent fields may reflect expected contextual features.…”

Section: A Role For Place Fields In Context Discriminationmentioning

confidence: 99%

Hippocampal place cells, context, and episodic memory

2006

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ABSTRACT:Although most observers agree that the hippocampus has a critical role in learning and memory, there remains considerable debate about the precise functional contribution of the hippocampus to these processes. Two of the most influential accounts hold that the primary function of the hippocampus is to generate cognitive maps and to mediate episodic memory processes. The well-documented spatial firing patterns (place fields) of hippocampal neurons in rodents, along with the spatial learning impairments observed with hippocampal damage support the cognitive mapping hypothesis. The amnesia for personally experienced events seen in humans with hippocampal damage and the data of animal models, which show severe memory deficits associated with hippocampal lesions, support the episodic memory account. Although an extensive literature supports each of these hypotheses, a specific contribution of place cells to episodic memory has not been clearly demonstrated. Recent data from our laboratory, together with previous findings, indicate that hippocampal place fields and neuronal responses to task-relevant stimuli are highly sensitive to the context, even when the contexts are defined by abstract task demands rather than the spatial geometry of the environment. On the basis of these findings, it is proposed that place fields reflect a more general context processing function of the hippocampus. Hippocampal context representations could serve to differentiate contexts and prime the relevant memories and behaviors. Since episodic memories, by definition, include information about the time and place where the episode occurred, contextual information is a necessary prerequisite for any episodic memory. Thus, place fields contribute importantly to episodic memory as part of the needed context representations. Additionally, recent findings indicate that hippocampal neurons differentiate contexts at progressively finer levels of detail, suggesting a hierarchical coding scheme which, if combined with temporal information, could provide a means of differentiating memory episodes. V V C 2006 Wiley-Liss, Inc.

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Distinct Ensemble Codes in Hippocampal Areas CA3 and CA1

Cited by 709 publications

References 32 publications

Updating hippocampal representations: CA2 joins the circuit

Updating hippocampal representations: CA2 joins the circuit

Multiple repetitions reveal functionally and anatomically distinct patterns of hippocampal activity during continuous recognition memory

Hippocampal place cells, context, and episodic memory

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