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Why there are Complementary Learning Systems in the Hippocampus and Neocortex: Insights from the Successes and Failures of Connectionist Models of Learning and Memory
, 1994
"... The influence of prior experience on some forms of behavior and cognition is drastically affected by damage to the hippocampal system. However, if the hippocampal system is left intact both during the experience and for a period of time thereafter, subsequent damage can have much less or even no eff ..."
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Cited by 288 (34 self)
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The influence of prior experience on some forms of behavior and cognition is drastically affected by damage to the hippocampal system. However, if the hippocampal system is left intact both during the experience and for a period of time thereafter, subsequent damage can have much less or even no effect. Such findings suggest that memory traces change over time in a way that makes them less dependent on the hippocampal system. This process of change has often been called consolidation. Consolidation is a very gradual process; in humans, it appears to span up to 15 years. This article asks what consolidation is and why it occurs. We take as our point of departure the view that the initial memory trace that results from a relevant experience consists of changes to the strengths of the connections among neurons in the hippocampal system. Bidirectional connections between the neocortex and the hippocampus allow these initial traces to mediate the reinstatement of representations of events o...
Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: A theory
- J. Neurosci
, 1996
"... The head-direction (HD) cells found in the limbic system in freely moving rats represent the instantaneous head direction of the animal in the horizontal plane regardless of the location of the animal. The internal direction represented by these cells uses both self-motion information for inet-tiall ..."
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Cited by 94 (1 self)
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The head-direction (HD) cells found in the limbic system in freely moving rats represent the instantaneous head direction of the animal in the horizontal plane regardless of the location of the animal. The internal direction represented by these cells uses both self-motion information for inet-tially based updating and familiar visual landmarks for calibration. Here, a model of the dynamics of the HD cell ensemble is presented. The sta-bility of a localized static activity profile in the network and a dynamic shift mechanism are explained naturally by synaptic weight distribution components with even and odd symmetry, respectively. Under symmetric weights or symmetric reciprocal connections, a stable activity profile close to the known direc-tional tuning curves will emerge. By adding a slight asymmetry to the weights, the activity profile will shift continuously without 1
Hippocampal Conjunctive Encoding, Storage, and Recall: Avoiding a Trade-Off
, 1994
"... The hippocampus and related structures are thought to be capable of 1) representing cortical activity in a way that minimizes overlap of the representations assigned t ~ different cortical patterns (pattern separation); and 2) modifying synaptic connections so that these representations can later be ..."
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Cited by 78 (15 self)
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The hippocampus and related structures are thought to be capable of 1) representing cortical activity in a way that minimizes overlap of the representations assigned t ~ different cortical patterns (pattern separation); and 2) modifying synaptic connections so that these representations can later be reinstated from partial or noisy versions of the cortical activity pattern that was present at the time of storage (pattern completion). We point out that there is a trade-off between pattern separation and completion and propose that the unique anatomical and physiological properties of the hippocampus might serve to minimize this trade-off. We use analytical methods to determine quantitative estimates of both separation and completion for specified parameterized models of the hippocampus. These estimates are then used to evaluate the role of various properties and of the hippocampus, such as the activity levels seen in different hippocampal regions, synaptic potentiation and depression, the multi-layer connectivity of the system, and the relatively focused and strong mossy fiber projections. This analysis is focused on the feedforward pathways from the entorhinal cortex (EC) to the dentate gyrus (DG) and region CA3. Among our results are the following: 1) Hebbian synaptic modification (LTP) facilitates completion but reduces separation, unless the
A model of hippocampal function
, 1994
"... The firing rate maps of hippocampal place cells recorded in a freely moving rat are viewed as a set of approximate radial basis functions over the (2-D) environment of the rat. It is proposed that these firing fields are constructed during exploration from 'sensory inputs' (tuning curve responses ..."
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Cited by 61 (6 self)
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The firing rate maps of hippocampal place cells recorded in a freely moving rat are viewed as a set of approximate radial basis functions over the (2-D) environment of the rat. It is proposed that these firing fields are constructed during exploration from 'sensory inputs' (tuning curve responses to the distance of cues from the rat) and used by cells downstream to construct firing rate maps that approximate any desired surface over the environment. It is shown that, when a rat moves freely in an open field, the phase of firing of a place cell (with respect to the EEG 0 rhythm) contains information as to the relative position of its firing field from the rat. A model of hippocampal function is presented in which the firing rate maps of cells downstream of the hippocampus provide a 'population vector' encoding the instantaneous direction of the rat from a previously encountered reward site, enabling navigation to it. A neuronal simulation, involving reinforcement only at the goal location, provides good agreement with single cell recording from the hippocampal region, and can navigate to reward sites in open fields using sensory input from environmental cues. The system requires only brief exploration, performs latent learning, and can return to a goal location after encountering it only once.
Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells
- J. Neumphysiol
, 1998
"... such as the orientation of a line in the visual field or the location of Two main goals for reconstruction are approached in this the body in space are coded as activity levels in populations of neurons. Reconstruction or decoding is an inverse problem in which paper. The first goal is technical and ..."
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Cited by 59 (5 self)
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such as the orientation of a line in the visual field or the location of Two main goals for reconstruction are approached in this the body in space are coded as activity levels in populations of neurons. Reconstruction or decoding is an inverse problem in which paper. The first goal is technical and is exemplified by the the physical variables are estimated from observed neural activity. population vector method applied to motor cortical activities Reconstruction is useful first in quantifying how much information during various reaching tasks (Georgopoulos et al. 1986, 1989; about the physical variables is present in the population and, second, Schwartz 1994) and the template matching method applied to in providing insight into how the brain might use distributed represen- disparity selective cells in the visual cortex (Lehky and Sejnowtations in solving related computational problems such as visual ob- ski 1990) and hippocampal place cells during rapid learning of ject recognition and spatial navigation. Two classes of reconstruction place fields in a novel environment (Wilson and McNaughton methods, namely, probabilistic or Bayesian methods and basis func- 1993). In these examples, reconstruction extracts information tion methods, are discussed. They include important existing methods from noisy neuronal population activity and transforms it to a
A Distributed Representation of Temporal Context
, 2002
"... The principles of recency and contiguity are two cornerstones of the theoretical and empirical analysis of human memory. Recency has been alternatively explained by mechanisms of decay, displacement, and retroactive interference. Another account of recency is based on the idea of variable context (E ..."
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Cited by 55 (16 self)
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The principles of recency and contiguity are two cornerstones of the theoretical and empirical analysis of human memory. Recency has been alternatively explained by mechanisms of decay, displacement, and retroactive interference. Another account of recency is based on the idea of variable context (Estes, 1955; Mensink & Raaijmakers, 1989). Such notions are typically cast in terms of a randomly fluctuating population of elements reflective of subtle changes in the environment or in the subjects ’ mental state. This random context view has recently been incorporated into distributed and neural network memory models (Murdock, 1997; Murdock, Smith, & Bai, 2001). Here we propose an alternative model. Rather than being driven by random fluctuations, this formulation, the temporal context model (TCM), uses retrieval of prior contextual states to drive contextual drift. In TCM, retrieved context is an inherently asymmetric retrieval cue. This allows the model to provide a principled explanation of the widespread advantage for forward recalls in free and serial recall. Modeling data from single-trial free recall, we demonstrate that TCM can simultaneously explain recency and
Probabilistic Interpretation of Population Codes
, 1998
"... We present a general encoding-decoding framework for interpreting the activity of a population of units. A standard population code interpretation method, the Poisson model, starts from a description as to how a single value of an underlying quantity can generate the activities of each unit in the p ..."
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Cited by 53 (9 self)
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We present a general encoding-decoding framework for interpreting the activity of a population of units. A standard population code interpretation method, the Poisson model, starts from a description as to how a single value of an underlying quantity can generate the activities of each unit in the population. In casting it in the encoding-decoding framework, we find that this model is too restrictive to describe fully the activities of units in population codes in higher processing areas, such as the medial temporal area. Under a more powerful model, the population activity can convey information not only about a single value of some quantity but also about its whole distribution, including its variance, and perhaps even the certainty the system has in the actual presence in the world of the entity generating this quantity. We propose a novel method for forming such probabilistic interpretations of population codes and compare it to the existing method.
Spatial Cognition and Neuro-Mimetic Navigation: A Model of Hippocampal Place Cell Activity
, 2000
"... . A computational model of hippocampal activity during spatial cognition and navigation tasks is presented. The spatial representation in our model of the rat hippocampus is built on-line during exploration via two processing streams. An allothetic vision-based representation is built by unsupervise ..."
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Cited by 52 (13 self)
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. A computational model of hippocampal activity during spatial cognition and navigation tasks is presented. The spatial representation in our model of the rat hippocampus is built on-line during exploration via two processing streams. An allothetic vision-based representation is built by unsupervised Hebbian learning extracting spatio-temporal properties of the environment from visual input. An idiothetic representation is learned based on internal movement-related information provided by path integration. On the level of the hippocampus, allothetic and idiothetic representations are integrated to yield a stable representation of the environment by a population of localized overlapping CA3-CA1 place fields. The hippocampal spatial representation is used as a basis for goal-oriented spatial behavior. We focus on the neural pathway connecting the hippocampus to the nucleus accumbens. Place cells drive a population of locomotor action neurons in the nucleus accumbens. Reward-based learnin...
Deciphering the hippocampal polyglot: The hippocampus as a path integration system
- Journal of Experimental Biology
, 1996
"... Hippocampal ‘place ’ cells and the head-direction cells of the dorsal presubiculum and related neocortical and thalamic areas appear to be part of a preconfigured network that generates an abstract internal representation of two-dimensional space whose metric is self-motion. It appears that viewpoin ..."
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Cited by 49 (3 self)
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Hippocampal ‘place ’ cells and the head-direction cells of the dorsal presubiculum and related neocortical and thalamic areas appear to be part of a preconfigured network that generates an abstract internal representation of two-dimensional space whose metric is self-motion. It appears that viewpoint-specific visual information (e.g. landmarks) becomes secondarily bound to this structure by associative learning. These associations between landmarks and the preconfigured path integrator serve to set the origin for path integration and to correct for cumulative
Statistically Efficient Estimation Using Population Coding
, 1998
"... Coarse codes are widely used throughout the brain to encode sensory and motor variables. Methods designed to interpret these codes, such as population vector analysis, are either inefficient (the variance of the estimate is much larger than the smallest possible variance) or biologically implausible ..."
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Cited by 46 (7 self)
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Coarse codes are widely used throughout the brain to encode sensory and motor variables. Methods designed to interpret these codes, such as population vector analysis, are either inefficient (the variance of the estimate is much larger than the smallest possible variance) or biologically implausible, like maximum likelihood. Moreover, these methods attempt to compute a scalar or vector estimate of the encoded variable. Neurons are faced with a similar estimation problem. They must read out the responses of the presynaptic neurons, but, by contrast, they typically encode the variable with a further population code rather than as a scalar. We show how a nonlinear recurrent network can be used to perform estimation in a near-optimal way while keeping the estimate in a coarse code format. This work suggests that lateral connections in the cortex may be involved in cleaning up uncorrelated noise among neurons representing similar variables.

