Latent Attractors: A Model for Context-Dependent Place Representations in the Hippocampus

Doboli, Simona; Minai, Ali A.; Best, Phillip J.

doi:10.1162/089976600300015484

Cited by 52 publications

(41 citation statements)

References 93 publications

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Section: Power Of the Number Of Intervening States (C-s)supporting

confidence: 77%

“…This is also consistent with the very sparse representations formed in these regions, as indicated by the relatively small number of active place cells in the dentate gyrus for a given environment (Jung and McNaughton, 1993). Previous models have also used dentate gyrus to provide context for CA1 unit activity (Doboli et al, 2000).Synaptic modification of region CA3 recurrent connections encodes associations between spiking induced by dentate gyrus input g c and dendritic depolarization caused by input from ECII: Where the matrix W ca3 represents strength of recurrent connections in region CA3 (starting from a small nonzero value) modified by activity in CA3 pyramidal cells. Presynaptic activity a ca3 is assumed to be dominated by spiking induced by mossy fiber inputs from the dentate gyrus, so presynaptic activity can be replaced with the distinct episodic representation formed in the dentate gyrus at each time step g c .…”

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confidence: 78%

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Hippocampal mechanisms for the context-dependent retrieval of episodes

2005

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Behaviors ranging from delivering newspapers to waiting tables depend on remembering previous episodes to avoid incorrect repetition. Physiologically, this requires mechanisms for long-term storage and selective retrieval of episodes based on time of occurrence, despite variable intervals and similarity of events in a familiar environment. Here, this process has been modeled based on physiological properties of the hippocampal formation, including mechanisms for sustained activity in entorhinal cortex and theta rhythm oscillations in hippocampal subregions. The model simulates the context-sensitive firing properties of hippocampal neurons including trial specific firing during spatial alternation and trial by trial changes in theta phase precession on a linear track. This activity is used to guide behavior, and lesions of the hippocampal network impair memory-guided behavior. The model links data at the cellular level to behavior at the systems level, describing a physiologically plausible mechanism for the brain to recall a given episode which occurred at a specific place and time.Keywords entorhinal cortex; dentate gyrus; region CA3; region CA1; spatial alternation; single unit recording; theta phase precession; current source density A waiter only takes orders once from each customer at each mealtime in a restaurant. Similarly, a foraging rat should avoid immediate return to a food cache where it just ate all the food. The ability to avoid repeating a completed behavior in a highly familiar environment depends on the ability to selectively retrieve recent episodes based on temporal context (e.g. in order to remember which customers or garbage cans were visited in a given time period).The context-sensitive properties of the spiking activity in the hippocampus may provide physiological mechanisms for this process. Some hippocampal neurons ("splitter cells" or "episodic cells") fire selectively dependent on the context of a specific recent response or future goal (Wood et al., 2000;Frank et al., 2000;Ferbinteanu and Shapiro, 2003). For example, during performance of a spatial alternation task, many hippocampal pyramidal neurons fire selectively after right turn or left turn trials, even though the rat is running in the same direction through the same location on the stem of the maze on both types of trials, as shown in Figure 1 (Wood et al., 2000). The model presented here shows how this activity may depend upon selective retrieval of prior episodes of behavior.During recordings on a linear track, other neurons show systematic changes in phase relative to theta frequency (7 Hz) oscillations in the hippocampal EEG (O'Keefe and Recce, 1993; Address correspondence to: Prof. Michael E. Hasselmo, Department of Psychology Center for Memory and Brain, Boston University, 2 Cummington St., Boston, MA 02215, (617) 353−1397, FAX: (617) Skaggs et al., 1996;Huxter et al., 2003). However, this theta phase precession does not appear on the first trial of the day, but appears on later trials of each day (Mehta ...

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Section: Power Of the Number Of Intervening States (C-s)supporting

confidence: 77%

supporting

confidence: 78%

Hippocampal mechanisms for the context-dependent retrieval of episodes

2005

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“…Neural activity in each of these states is focused on a relatively small, uniquely selected subpopulation of principal cells. Each state of this sort could possess certain (meta-) stability typical of a latent attractor state (Samsonovich and McNaughton 1997;Doboli et al 2000). The most commonly held account of the neural basis of contextual reinstatement is that PFC is used to access information in semantic memory (Shimamura 1995;Moscovitch 1992;Dobbins et al 2002) that is stored in MTL, and not in the hippocampus (Vargha-Khadem et al 1997) nor in PFC (e.g., Sylvester and Shimamura 2002).…”

Section: Understanding Hippocampal Function In Episodic Memory Retrievalmentioning

confidence: 99%

A simple neural network model of the hippocampus suggesting its pathfinding role in episodic memory retrieval

Samsonovich¹,

Ascoli²

2005

Learn. Mem.

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The goal of this work is to extend the theoretical understanding of the relationship between hippocampal spatial and memory functions to the level of neurophysiological mechanisms underlying spatial navigation and episodic memory retrieval. The proposed unifying theory describes both phenomena within a unique framework, as based on one and the same pathfinding function of the hippocampus. We propose a mechanism of reconstruction of the context of experience involving a search for a nearly shortest path in the space of remembered contexts. To analyze this concept in detail, we define a simple connectionist model consistent with available rodent and human neurophysiological data. Numerical study of the model begins with the spatial domain as a simple analogy for more complex phenomena. It is demonstrated how a nearly shortest path is quickly found in a familiar environment. We prove numerically that associative learning during sharp waves can account for the necessary properties of hippocampal place cells. Computational study of the model is extended to other cognitive paradigms, with the main focus on episodic memory retrieval. We show that the ability to find a correct path may be vital for successful retrieval. The model robustly exhibits the pathfinding capacity within a wide range of several factors, including its memory load (up to 30,000 abstract contexts), the number of episodes that become associated with potential target contexts, and the level of dynamical noise. We offer several testable critical predictions in both spatial and memory domains to validate the theory. Our results suggest that (1) the pathfinding function of the hippocampus, in addition to its associative and memory indexing functions, may be vital for retrieval of certain episodic memories, and (2) the hippocampal spatial navigation function could be a precursor of its memory function.The phenomenon of hippocampal spatial representations and the hippocampal role in episodic memory retrieval remain two of the most puzzling mysteries in cognitive neuroscience that intuitively seem to be connected to each other. Since the finding that the hippocampus plays a pivotal role in long-term memory consolidation (Scoville and Milner 1957; Zola-Morgan and Squire 1986), many proposals have been made regarding its specific role (Teyler and Discenna 1985;Squire 1987;O'Reilly and McClelland 1994;McClelland et al. 1995). A prominent view of the mechanisms underlying consolidation of episodic memories involves fast formation (e.g., via Hebbian mechanisms) of strong associations between hippocampal sparse patterns of activity and distributed neocortical representations. As a result, the former subsequently serve as pointers to the latter. This memory-indexing theory that goes back to Teyler andDiscenna (1985, 1986) and underlies several subsequent major theoretical contributions to the field (Nadel and Wheeler et al. 1997;Tulving 2002) assumes that a memory of an episode is retrieved by reactivating a hippocampal pointer to it. Consistent with this view, r...

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“…In this way, a given CA3 cell will fire in a particular place, but only in a particular context. For an alternate view on context representation, see Doboli et al (2000).…”

Section: Linkage Of Sequences With Context At Perforant Path Inputs Tmentioning

confidence: 99%

Storage, recall, and novelty detection of sequences by the hippocampus: Elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine

2001

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ABSTRACT:In order to understand how the molecular or cellular defects that underlie a disease of the nervous system lead to the observable symptoms, it is necessary to develop a large-scale neural model. Such a model must specify how specific molecular processes contribute to neuronal function, how neurons contribute to network function, and how networks interact to produce behavior. This is a challenging undertaking, but some limited progress has been made in understanding the memory functions of the hippocampus with this degree of detail. There is increasing evidence that the hippocampus has a special role in the learning of sequences and the linkage of specific memories to context. In the first part of this paper, we review a model (the SOCRATIC model) that describes how the dentate and CA3 hippocampal regions could store and recall memory sequences in context. A major line of evidence for sequence recall is the "phase precession" of hippocampal place cells. In the second part of the paper, we review the evidence for theta-gamma phase coding. According to a framework that incorporates this form of coding, the phase precession is interpreted as cued recall of a discrete sequence of items from long-term memory. The third part of the paper deals with the issue of how the hippocampus could learn memory sequences. We show that if multiple items can be active within a theta cycle through the action of a short-term "buffer," NMDA-dependent plasticity can lead to the learning of sequences presented at realistic item separation intervals. The evidence for such a buffer function is reviewed. An important underlying issue is whether the hippocampal circuitry is configured differently for learning and recall. We argue that there are indeed separate states for learning and recall, but that both involve theta oscillations, albeit in possibly different forms. This raises the question of how neuromodulatory input might switch the hippocampus between learning and recall states and more generally how different neuromodulatory inputs reconfigure the hippocampus for different functions. In the fifth part of this paper we review our studies of dopamine and dopamine/NMDA interactions in the control of synaptic function. Our results show that dopamine dramatically reduces the direct cortical input to CA1 (the perforant path input), while having little effect on the input from CA3. In order to interpret the functional consequences of this pathway-specific modulation, it is necessary to understand the function of CA1 and the role of dopaminergic input from the ventral tegmental area (VTA). In the sixth part of this paper we consider several possibilities and address the issue of how dopamine hyperfunction or NMDA hypofunction, abnormalities that may underlie schizophrenia, might lead to the symptoms of the disease. Relevant to this issue is the demonstrated role of the hippocampus in novelty detection, a function that is likely to depend on sequence recall by the hippocampus. Novelty signals are generated when reality does not match ...

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Latent Attractors: A Model for Context-Dependent Place Representations in the Hippocampus

Cited by 52 publications

References 93 publications

Hippocampal mechanisms for the context-dependent retrieval of episodes

Hippocampal mechanisms for the context-dependent retrieval of episodes

A simple neural network model of the hippocampus suggesting its pathfinding role in episodic memory retrieval

Storage, recall, and novelty detection of sequences by the hippocampus: Elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine

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