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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...
Rules and Exemplars in Category Learning
- Journal of Experimental Psychology: General
, 1998
"... haracterized by descriptions of each module and how each serves in those tasks for which it is best suited. However, these theories often do not emphasize how modules interact in producing responses and in learning. In this article we will develop a modular theory of categorization that follows fro ..."
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Cited by 92 (3 self)
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haracterized by descriptions of each module and how each serves in those tasks for which it is best suited. However, these theories often do not emphasize how modules interact in producing responses and in learning. In this article we will develop a modular theory of categorization that follows from two distinct accounts of this behavior. The first account is that of rule-based theories of categorization. These theories emerge from a philosophical tradition in which concepts and categorization are described in terms of definitional rules. For example, if a living thing has a wide, flat tail and constructs dams by cutting down trees with its This work was supported by Indiana University Cognitive Science Program Fellowships and by NIMH ResearchTraining Grant PHS-T32-MH19879-03 to Erickson, and in part by NIMH FIRST Award 1-R29-MH51572-01 to Kruschke. This research was reported as a poster at the 1996 Cognitive Science Society Conference in San Diego, CA. We than
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
Conjunctive Representations in Learning and Memory: Principles of Cortical and Hippocampal Function
- PSYCHOLOGICAL REVIEW
, 2001
"... We present a theoretical framework for understanding the roles of the hippocampus and neocortex in learning and memory. This framework incorporates a theme found in many theories of hippocampal function, that the hippocampus is responsible for developing conjunctive representations binding together ..."
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Cited by 59 (11 self)
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We present a theoretical framework for understanding the roles of the hippocampus and neocortex in learning and memory. This framework incorporates a theme found in many theories of hippocampal function, that the hippocampus is responsible for developing conjunctive representations binding together stimulus elements into a unitary rep- resentation that can later be recalled from partial input cues. This idea appears problematic, however, because it is contradicted by the fact that hippocampally lesioned rats can learn nonlinear discrimination problems that require conjunctive representations. Our framework accommodates this finding by establishing a principled division of labor between the cortex and hippocampus, where the cortex is responsible for slow learning that integrates over multiple experiences to extract generalities, while the hippocampus performs rapid learning of the arbitrary contents of individual experiences. This framework shows that nonlinear discrimination problems are not good tests of hippocampal function, and suggests that tasks involving rapid, incidental conjunctive learning are better. We implement this framework in a computational neural network model, and show that it can account for a wide range of data in animal learning, thus validating our theoretical ideas, and providing a number of insights and predictions about these learning phenomena.
Modeling hippocampal and neocortical contributions to recognition memory: A complementary-learning-systems approach
- Psychological Review
, 2003
"... We present a computational neural network model of recognition memory based on the biological structures of the hippocampus and medial temporal lobe cortex (MTLC), which perform complementary learning functions. The hippocampal component of the model contributes to recognition by recalling specific ..."
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Cited by 50 (10 self)
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We present a computational neural network model of recognition memory based on the biological structures of the hippocampus and medial temporal lobe cortex (MTLC), which perform complementary learning functions. The hippocampal component of the model contributes to recognition by recalling specific studied details. MTLC can not support recall, but it is possible to extract a scalar familiarity signal from MTLC that tracks how well the test item matches studied items. We present simulations that establish key qualitative differences in the operating characteristics of the hippocampal recall and MTLC familiarity signals, and we identify several manipulations (e.g., target-lure similarity, interference) that differentially affect the two signals. We also use the model to address the stochastic relationship between recall and familiarity (i.e., are they independent), and the effects of partial vs. complete hippocampal
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 50 (4 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
Dual-process models in social and cognitive psychology: Conceptual integration and links to underlying memory systems
- Personality and Social Psychology Review
, 2000
"... On behalf of: ..."
Dissociating explicit and procedural-learning based systems of perceptual category learning
, 2004
"... A fundamental question is whether people have available one category learning system, or many. Most multiple systems advocates postulate one explicit and one implicit system. Although there is much agreement about the nature of the explicit system, there is less agreement about the nature of the imp ..."
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Cited by 30 (18 self)
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A fundamental question is whether people have available one category learning system, or many. Most multiple systems advocates postulate one explicit and one implicit system. Although there is much agreement about the nature of the explicit system, there is less agreement about the nature of the implicit system. In this article, we review a dual systems theory of category learning called competition between verbal and implicit systems (COVIS) developed by Ashby et al. (1998). The explicit system dominates the learning of verbalizable, rule-based category structures and is mediated by frontal brain areas such as the anterior cingulate, prefrontal cortex (PFC), and head of the caudate nucleus. The implicit system, which uses procedural learning, dominates the learning of non-verbalizable, information-integration category structures, and is mediated by the tail of the caudate nucleus and a dopamine-mediated reward signal. We review nine studies that test six a priori predictions from COVIS, each of which is supported by the data.
The Role of the Hippocampus in Solving the Morris Water Maze
, 1997
"... this article. Because there is no visible cue in the hidden-platform water maze task, it would not help the animal find the platform. 3. Route system. Routes stored in the hippocampus can be written out to the cortex, so that directions necessary to reach a goal are associated with local views. This ..."
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Cited by 28 (2 self)
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this article. Because there is no visible cue in the hidden-platform water maze task, it would not help the animal find the platform. 3. Route system. Routes stored in the hippocampus can be written out to the cortex, so that directions necessary to reach a goal are associated with local views. This is the system detailed in section 2.5 (see also section 4.3). This system requires training for each step the animal must take; it cannot learn to associate local views with directions to distant goals without hippocampal help (through route replay). The Role of the Hippocampus 97 If there were a way to show the animal the route to the goal, it might be possible to train the route system even without a hippocampus. Whishaw, Cassell, and Jarrard (1995) and Schallert, Day, Weisend, and Sutherland (1996) both showed ways to train the route system directly and found that animals could learn to solve the water maze even with hippocampal lesions. Whishaw et al. (1995) trained animals with fimbria/fornix lesions to find a visible platform and then removed the visible platform. These animals concentrated their search where the platform had been. Schallert et al. (1996) used animals with kainate-colchicine hippocampal lesions. The animals were first trained with a large platform that filled almost the entire maze. Once the animals could reach that platform reliably, it was shrunk trial by trial until it was the same size as a typical platform in a water maze task. Again, the animals could learn to solve the water maze without a hippocampus. 4.3 Where Is the Route System? Although the data are not yet conclusive, we suggest that the most likely candidate for anatomical instantiation of the route system is from posterior parietal to posterior cingulate cortex. There is a lot of evide...
Similarities and Differences in the Neural Correlates of Episodic Memory Retrieval And Working Memory
- Neuroimage
, 2002
"... erations, respectively; and (iii) left posterior/ventral (Broca's area) and bilateral posterior/dorsal areas were more activated during WM than during ER, possibly reflecting phonological and generic WM operations, respectively. Second, hippocampal and parahippocampal regions were activated not only ..."
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Cited by 27 (4 self)
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erations, respectively; and (iii) left posterior/ventral (Broca's area) and bilateral posterior/dorsal areas were more activated during WM than during ER, possibly reflecting phonological and generic WM operations, respectively. Second, hippocampal and parahippocampal regions were activated not only for ER but also for WM. This result suggests that indexing operations mediated by the medial temporal lobes apply to both long-term and short-term memory traces. Overall, our results show that direct cross-function comparisons are critical to understand the role of different brain regions in various cognitive functions. 2002 Elsevier Science (USA) INTRODUCTION During the past decade, numerous positron emission tomography (PET) and functional MRI (fMRI) studies have investigated the neural correlates of different cognitive functions (for a review, see Cabeza and Nyberg, 2000). Although most studies have focused on a single function (see however, LaBar et al., 1999; Braver et al., 2001; Ny

