Context representations, context functions, and the parahippocampal–hippocampal system

Rudy, Jerry W.

doi:10.1101/lm.1494409

PreprintCited by 296Memory and Neural MechanismsMemory Processes and InfluencesNeurogenesis and neuroplasticity mechanisms

Context representations, context functions, and the parahippocampal–hippocampal system

Open access

Rudy, Jerry W.·2009·Learning & Memory

DOI 10.1101/lm.1494409PMC PMC2769166

Open this paper in CoChat — free account Open PDF

Abstract

Psychologists and neurobiologists have a long-standing interest in understanding how the context surrounding the events of our lives is represented and how it influences our behavior. The hippocampal formation emerged very early as a major contributor to how context is represented and functions. There is a large literature examining its contribution that on the surface reveals an array of conflicting outcomes and controversy. This review reveals that these conflicts can be resolved by building Nadel and Willner's dual-process theory of context representations. Two general conclusions emerge: (1) There are two neural systems that can support context representations and functions-a neocortical system composed primarily of perirhinal and postrhinal cortices and a hippocampal system that includes perirhinal, postrhinal, entorhinal cortices, and the hippocampal formation. (2) These two systems are not equivalent-some context representations and functions are uniquely supported by the hippocampal system. These conclusions are discussed in the context of canonical ideas about the special properties of the hippocampal system that enable it to make unique contributions to memory.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1101/lm.1494409

Cites

131 of 131 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

The hippocampus helps encode episodic and emotional information that arises during motivationally relevant events.
“Likewise, the hippocampus, known for its contextual sensitivity (Fanselow, 2010; Hirsh, 1974, Rudy, 2009, Fanselow, 2010), helps encode episodic and emotional information that arises during motivationally relevant events.”
From Adolescent neurobiological susceptibility to social context (2016) · cites this paper as Rudy, 2009

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Untitled work
(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010 · see citing works
A theory of Pavlovian conditioning : Variations in the effectiveness of reinforcement and nonreinforcement
Rescorla, R. A. (1972) · Medical Entomology and Zoology · Cited by 7,268 · see citing works
Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans.
Squire, L. R. (1992) · Psychological Review · doi:10.1037/0033-295x.99.2.195 · Cited by 5,376 · see citing works
Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory
McClelland, J. L., McNaughton, B. L., & O'Reilly, R. C. (1995) · Psychological Review · doi:10.1037/0033-295x.102.3.419 · Cited by 5,256 · see citing works
Episodic memory: from mind to brain
Tulving, E. (2002) · Annual Review of Psychology · doi:10.1146/annurev.psych.53.100901.135114 · Cited by 4,950 · see citing works
Classical conditioning II: Current research and theory.
Black, A. H., & Prokasy, W. F. (1972) · Appleton-Century-Crofts eBooks · Cited by 4,449 · see citing works
Contributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior
Phelps, E. A., & LeDoux, J. E. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.025 · Cited by 3,203 · cited 1× · see citing works
“Moreover, there is a known neural circuit in the amygdala complex that supports this behavioral system (LeDoux 1994, 1995; Maren 2003; Phelps and LeDoux 2005; Davis 2006).”
Background
Simple memory: a theory for archicortex
Marr, D. (1971) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1971.0078 · Cited by 2,771 · see citing works
Memory consolidation, retrograde amnesia and the hippocampal complex
Nadel, L., & Moscovitch, M. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80010-4 · Cited by 1,924 · see citing works
Context, time, and memory retrieval in the interference paradigms of Pavlovian learning
Bouton, M. E. (1993) · Psychological Bulletin · doi:10.1037/0033-2909.114.1.80 · Cited by 1,896 · see citing works
Context and Behavioral Processes in Extinction: Table 1.
Bouton, M. E. (2004) · Learning & Memory · doi:10.1101/lm.78804 · Cited by 1,808 · see citing works
A cortical–hippocampal system for declarative memory
Eichenbaum, H. (2000) · Nature reviews. Neuroscience · doi:10.1038/35036213 · Cited by 1,725 · see citing works
Emotion: Clues from the Brain
LeDoux, J. E. (1995) · Annual Review of Psychology · doi:10.1146/annurev.ps.46.020195.001233 · Cited by 1,646 · see citing works
Species-specific defense reactions and avoidance learning
Bolles, R. C. (1970) · Psychological Review · doi:10.1037/h0028589 · Cited by 1,610 · see citing works
Memory, amnesia, and the hippocampal system
(1994) · Choice Reviews Online · doi:10.5860/choice.31-5148 · Cited by 1,533 · see citing works
Hippocampal synaptic enhancement and information storage within a distributed memory system
McNaughton, B. L., & Morris, R. G. M. (1987) · Trends in Neurosciences · doi:10.1016/0166-2236(87)90011-7 · Cited by 1,304 · see citing works
Cortical pathways to the mammalian amygdala
McDonald, A. J. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00003-3 · Cited by 1,303 · see citing works
The anatomy of memory: an interactive overview of the parahippocampal–hippocampal network
van Strien, N. M., Cappaert, N. L. M., & Witter, M. P. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2614 · Cited by 1,041 · see citing works
The hippocampus and contextual retrieval of information from memory: A theory
Hirsh, R. (1974) · Behavioral Biology · doi:10.1016/s0091-6773(74)92231-7 · Cited by 957 · see citing works
Configural association theory: The role of the hippocampal formation in learning, memory, and amnesia
Sutherland, R. J., & Rudy, J. W. (1989) · Psychobiology · doi:10.3758/bf03337828 · Cited by 956 · see citing works
Self-citation
Hippocampal conjunctive encoding, storage, and recall: Avoiding a trade‐off
O'Reilly, R. C., & McClelland, J. L. (1994) · Hippocampus · doi:10.1002/hipo.450040605 · Cited by 914 · see citing works
Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys
Meunier, M., Bachevalier, J., Mishkin, M., & Murray, E. A. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-12-05418.1993 · Cited by 900 · see citing works
Emotion, Memory and the Brain
LeDoux, J. E. (1994) · Scientific American · doi:10.1038/scientificamerican0694-50 · Cited by 892 · see citing works
The hippocampal memory indexing theory.
Teyler, T. J., & DiScenna, P. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.2.147 · Cited by 871 · see citing works
Conjunctive representations in learning and memory: Principles of cortical and hippocampal function.
O'Reilly, R. C., & Rudy, J. W. (2001) · Psychological Review · doi:10.1037//0033-295x.108.2.311 · Cited by 865 · see citing works
Self-citation
Contextual control of the extinction of conditioned fear
Bouton, M. E., & Bolles, R. C. (1979) · Learning and Motivation · doi:10.1016/0023-9690(79)90057-2 · Cited by 796 · see citing works
Latent inhibition.
Lubow, R. E. (1973) · Psychological Bulletin · doi:10.1037/h0034425 · Cited by 793 · see citing works
Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats
Maren, S., Aharonov, G., & Fanselow, M. S. (1997) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00088-0 · Cited by 765 · see citing works
Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts
Mumby, D. G., Gaskin, S., Glenn, M. J., Schramek, T. E., & Lehmann, H. (2002) · Learning & Memory · doi:10.1101/lm.41302 · Cited by 714 · see citing works
Extending the spontaneous preference test of recognition: evidence of object-location and object-context recognition
Dix, S. L., & Aggleton, J. P. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00079-5 · Cited by 598 · see citing works
Neural systems involved in fear and anxiety measured with fear-potentiated startle.
Davis, M. (2006) · American Psychologist · doi:10.1037/0003-066x.61.8.741 · Cited by 589 · see citing works
Factors governing one-trial contextual conditioning
Fanselow, M. S. (1990) · Animal Learning & Behavior · doi:10.3758/bf03205285 · Cited by 564 · see citing works
The Parahippocampal Region: Corticocortical Connectivity
Burwell, R. D. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06717.x · Cited by 513 · see citing works
The dorsal hippocampus is essential for context discrimination but not for contextual conditioning.
Frankland, P. W., Cestari, V., Filipkowski, R. K., McDonald, R. J., & Silva, A. J. (1998) · Behavioral Neuroscience · doi:10.1037//0735-7044.112.4.863 · Cited by 486 · see citing works
Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory
Morris, R., Moser, E. I., Riedel, G., Martin, S. J., Sandin, J., Day, M., & O’Carroll, C. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1264 · Cited by 480 · see citing works
Hippocampal Inactivation Disrupts Contextual Retrieval of Fear Memory after Extinction
Corcoran, K. A., & Maren, S. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01720.2001 · Cited by 455 · cited 1× · see citing works
“In contrast to Bouton’s findings, Maren and colleagues (Corcoran and Maren 2001, 2004; Corcoran et al. 2005; Ji and Maren 2005; Hobin et al. 2006) report that context-specific extinction does require a contribution of the hippocampal formation.”
Result
The dorsal hippocampus is essential for context discrimination but not for contextual conditioning.
Frankland, P. W., Cestari, V., Filipkowski, R. K., et al. (1998) · Behavioral Neuroscience · doi:10.1037/0735-7044.112.4.863 · Cited by 435 · see citing works
Rhinal cortex lesions and object recognition in rats.
Mumby, D. G., & Pinel, J. P. J. (1994) · Behavioral Neuroscience · doi:10.1037//0735-7044.108.1.11 · Cited by 412 · see citing works
The Midbrain Periaqueductal Gray as a Coordinator of Action in Response to Fear and Anxiety
Fanselow, M. S. (1991) · Springer eBooks · doi:10.1007/978-1-4615-3302-3_10 · Cited by 405 · see citing works
Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas
Morris, R. G. M. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04888.x · Cited by 398 · see citing works
Double dissociation of function within the hippocampus: A comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions
Bannerman, D. M., Yee, B. K., Good, M. A., Heupel, M. J., Iversen, S. D., & Rawlins, J. N. P. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.6.1170 · Cited by 397 · see citing works
Hippocampal Inactivation Disrupts the Acquisition and Contextual Encoding of Fear Extinction
Corcoran, K., Desmond, T., Frey, K., & Maren, S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2246-05.2005 · Cited by 390 · see citing works
Context and Learning
Balsam, P. D., & Tomie, A. (2014) · Psychology Press eBooks · doi:10.4324/9781315802466 · Cited by 389 · see citing works
Context and conditioning: A place for space
Nadel, L., & Willner, J. (1980) · Physiological Psychology · doi:10.3758/bf03332853 · Cited by 373 · see citing works
The hippocampal indexing theory and episodic memory: Updating the index
Teyler, T. J., & Rudy, J. W. (2007) · Hippocampus · doi:10.1002/hipo.20350 · Cited by 373 · see citing works
Self-citation
The Role of the Dorsal Hippocampus in the Acquisition and Retrieval of Context Memory Representations
Matus-Amat, P., Higgins, E. A., Barrientos, R., & Rudy, J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1598-03.2004 · Cited by 358 · see citing works
Self-citation
Context Fear Learning in the Absence of the Hippocampus
Wiltgen, B. J., Sanders, M. J., Anagnostaras, S., Sage, J. R., & Fanselow, M. S. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2685-05.2006 · Cited by 349 · see citing works
Rhinal cortex lesions and object recognition in rats.
Mumby, D. G., & Pinel, J. P. J. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.1.11 · Cited by 348 · see citing works
Integrated Memory for Object, Place, and Context in Rats: A Possible Model of Episodic-Like Memory?
Eacott, M. J., & Norman, G. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2975-03.2004 · Cited by 344 · see citing works
Selective hippocampal lesions abolish the contextual specificity of latent inhibition and conditioning.
Honey, R. C., & Good, M. A. (1993) · Behavioral Neuroscience · doi:10.1037//0735-7044.107.1.23 · Cited by 336 · see citing works
Dissociating context and space within the hippocampus: Effects of complete, dorsal, and ventral excitotoxic hippocampal lesions on conditioned freezing and spatial learning.
Richmond, M. A., Yee, B. K., Pouzet, B., Veenman, L., Rawlins, J. N. P., Feldon, J., & Bannerman, D. M. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.6.1189 · Cited by 332 · see citing works
Neuroscience and Connectionist Theory
Gluck, M. A., & Rumelhart, D. E. (2013) · Psychology Press eBooks · doi:10.4324/9780203762981 · Cited by 320 · see citing works
The place of the hippocampus in fear conditioning
Sanders, M. J., Wiltgen, B. J., & Fanselow, M. S. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01283-4 · Cited by 316 · see citing works
Hippocampal place cells, context, and episodic memory
Smith, D. M., & Mizumori, S. J. Y. (2006) · Hippocampus · doi:10.1002/hipo.20208 · Cited by 302 · see citing works
Hippocampal involvement in contextual modulation of fear extinction
Ji, J., & Maren, S. (2007) · Hippocampus · doi:10.1002/hipo.20331 · Cited by 297 · see citing works
Selective association and conditioning
Kamin, L. J. (1969) · Medical Entomology and Zoology · Cited by 285 · see citing works
Transient Inactivation of Perirhinal Cortex Disrupts Encoding, Retrieval, and Consolidation of Object Recognition Memory
Winters, B. D., & Bussey, T. J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3827-04.2005 · Cited by 283 · see citing works
Functional neuroanatomy of the parahippocampal region in the rat: The perirhinal and postrhinal cortices
Furtak, S. C., Wei, S., Agster, K. L., & Burwell, R. D. (2007) · Hippocampus · doi:10.1002/hipo.20314 · Cited by 282 · see citing works
Hippocampal formation supports conditioning to memory of a context.
Rudy, J. W., Barrientos, R. M., & O’Reilly, R. C. (2002) · Behavioral Neuroscience · doi:10.1037//0735-7044.116.4.530 · Cited by 280 · see citing works
Self-citation
Contextual fear conditioning, conjunctive representations, pattern completion, and the hippocampus.
Rudy, J. W., & O’Reilly, R. C. (1999) · Behavioral Neuroscience · doi:10.1037//0735-7044.113.5.867 · Cited by 279 · see citing works
Self-citation
Selective hippocampal lesions abolish the contextual specificity of latent inhibition and conditioning.
Honey, R. C., & Good, M. A. (1993) · Behavioral Neuroscience · doi:10.1037/0735-7044.107.1.23 · Cited by 274 · see citing works
Glutamate-receptor-mediated encoding and retrieval of paired-associate learning
Day, M., Langston, R. F., & Morris, R. (2003) · Nature · doi:10.1038/nature01769 · Cited by 259 · see citing works
Conjunctive representations, the hippocampus, and contextual fear conditioning
RUDY, J. W., & O'REILLY, R. C. (2001) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/cabn.1.1.66 · Cited by 247 · see citing works
Self-citation
Hebb-Marr Networks and the Neurobiological Representation of Action in Space
Gluck, M. A., & Rumelhart, D. E. (2013) · Psychology Press eBooks · doi:10.4324/9780203762981-6 · Cited by 246 · see citing works
Ontogeny of contextual fear conditioning in rats: Implications for consolidation, infantile amnesia, and hippocampal system function.
Rudy, J. W., & Morledge, P. (1994) · Behavioral Neuroscience · doi:10.1037//0735-7044.108.2.227 · Cited by 245 · see citing works
Self-citation
Hippocampal formation supports conditioning to memory of a context.
Rudy, J. W., Barrientos, R. M., & O’Reilly, R. C. (2002) · Behavioral Neuroscience · doi:10.1037/0735-7044.116.4.530 · Cited by 242 · see citing works
Self-citation
Dissociation Between the Effects of Damage to Perirhinal Cortex and Area TEPreprint
Buffalo, E. A., Ramus, S. J., Clark, R. E., Teng, E., Squire, L. R., & Zola, S. M. (1999) · Learning & Memory · doi:10.1101/lm.6.6.572 · Cited by 241 · see citing works
Contextual fear conditioning, conjunctive representations, pattern completion, and the hippocampus.
Rudy, J. W., & O’Reilly, R. C. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.5.867 · Cited by 240 · see citing works
Self-citation
Learning-Related Development of Context-Specific Neuronal Responses to Places and Events: The Hippocampal Role in Context Processing
Smith, D. M., & Mizumori, S. J. Y. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3234-05.2006 · Cited by 234 · see citing works
Dissociable Effects of Lesions to the Perirhinal Cortex and the Postrhinal Cortex on Memory for Context and Objects in Rats.
Norman, G., & Eacott, M. J. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.2.557 · Cited by 217 · see citing works
Muscimol Inactivation of the Dorsal Hippocampus Impairs Contextual Retrieval of Fear Memory
Holt, W., & Maren, S. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-20-09054.1999 · Cited by 213 · see citing works
Learning and memory
Alkon, D. L., Amaral, D. G., Bear, M. F., Black, J., Carew, T. J., Cohen, N. J., Disterhoft, J. F., Eichenbaum, H., Golski, S., Gorman, L. K., et al. (1991) · Brain Research Reviews · doi:10.1016/0165-0173(91)90005-s · Cited by 212 · see citing works
Ventral hippocampal muscimol disrupts context‐specific fear memory retrieval after extinction in rats
Hobin, J. A., Ji, J.-Z., & Maren, S. (2006) · Hippocampus · doi:10.1002/hipo.20144 · Cited by 211 · see citing works
Ontogeny of contextual fear conditioning in rats: Implications for consolidation, infantile amnesia, and hippocampal system function.
Rudy, J. W., & Morledge, P. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.2.227 · Cited by 207 · see citing works
Self-citation
Effects of the novelty or familiarity of visual stimuli on the expression of the immediate early gene c-fos in rat brain
Zhu, X. O., Brown, M. W., McCabe, B. J., & Aggleton, J. P. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00320-i · Cited by 205 · see citing works
Projection neurons of the basolateral amygdala: A correlative Golgi and retrograde tract tracing study
McDonald, A. J. (1992) · Brain Research Bulletin · doi:10.1016/0361-9230(92)90177-y · Cited by 194 · see citing works
Neuronal Sianallina of Information Imoortant to Visual Recognition‐Memory in Rat Rhinal aid Neighbouring Cortices
Zhu, X. O., Brown, M. W., & Aggleton, J. P. (1995) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1995.tb00679.x · Cited by 194 · see citing works
The hippocampus, conditional operations, and cognition
Hirsh, R. (1980) · Physiological Psychology · doi:10.3758/bf03332848 · Cited by 192 · see citing works
Retrograde amnesia after hippocampal damage: Recent vs. remote memories in two tasks
Sutherland, R. J., Weisend, M. P., Mumby, D. G., Astur, R. S., Hanlon, F. M., Koerner, A., Thomas, M. J., Wu, Y., Moses, S. N., Cole, C., et al. (2001) · Hippocampus · doi:10.1002/1098-1063(2001)11:1 · Cited by 190 · see citing works
Dissociable effects of selective lesions to hippocampal subsystems on exploratory behavior, contextual learning, and spatial learning.
Good, M. A., & Honey, R. C. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.3.487 · Cited by 187 · see citing works
Factors regulating the effects of hippocampal inactivation on renewal of conditional fear after extinction.Preprint
Corcoran, K., & Maren, S. (2004) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.78704 · Cited by 182 · see citing works
Hippocampus, context, and conditioning.
Penick, S., & Solomom, P. R. (1991) · Behavioral Neuroscience · doi:10.1037//0735-7044.105.5.611 · Cited by 178 · see citing works
Electrolytic lesions of the dorsal hippocampus disrupt renewal of conditional fear after extinction.Preprint
Ji, J.-Z., & Maren, S. (2005) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.91705 · Cited by 174 · see citing works
Amygdala, hippocampus and discriminative fear conditioning to context
Antoniadis, E. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00121-7 · Cited by 170 · see citing works
Extensive Cytotoxic Lesions Involving Both the Rhinal Cortices and Area TE Impair Recognition But Spare Spatial Alternation in the Rat
Aggleton, J. P., Keen, S., Warburton, E. C., & Bussey, T. J. (1997) · Brain Research Bulletin · doi:10.1016/s0361-9230(97)00007-5 · Cited by 168 · see citing works
The Amygdala, Synaptic Plasticity, and Fear Memory
Maren, S. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07075.x · Cited by 159 · see citing works
Contributions of postrhinal and perirhinal cortex to contextual information processing.
Bucci, D. J., Phillips, R. G., & Burwell, R. D. (2021) · Behavioral Neuroscience · doi:10.1037/bne0000436 · Cited by 154 · see citing works
Neurotoxic or electrolytic lesions of the ventral subiculum produce deficits in the acquisition and expression of Pavlovian fear conditioning in rats.
Maren, S. (1999) · Behavioral Neuroscience · doi:10.1037//0735-7044.113.2.283 · Cited by 153 · see citing works
Dissociable effects of selective lesions to hippocampal subsystems on exploratory behavior, contextual learning, and spatial learning.
Good, M. A., & Honey, R. C. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.3.487 · Cited by 149 · see citing works
The Ventral Hippocampus Supports a Memory Representation of Context and Contextual Fear Conditioning: Implications for a Unitary Function of the Hippocampus.
Rudy, J. W., & Matus-Amat, P. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.1.154 · Cited by 147 · see citing works
Self-citation
Disruptive effects of posttraining perirhinal cortex lesions on conditioned fear: Contributions of contextual cues.
Corodimas, K. P., & LeDoux, J. E. (1995) · Behavioral Neuroscience · doi:10.1037//0735-7044.109.4.613 · Cited by 145 · see citing works
Hippocampus, context, and conditioning.
Penick, S., & Solomom, P. R. (1991) · Behavioral Neuroscience · doi:10.1037/0735-7044.105.5.611 · Cited by 144 · see citing works
The role of the rat hippocampal system in several effects of context in extinction.
Wilson, A., Brooks, D. C., & Bouton, M. E. (1995) · Behavioral Neuroscience · doi:10.1037//0735-7044.109.5.828 · Cited by 140 · see citing works
The precision of remote context memories does not require the hippocampus
Wang, S., Teixeira, C. M., Wheeler, A. L., & Frankland, P. W. (2009) · Nature Neuroscience · doi:10.1038/nn.2263 · Cited by 138 · see citing works
Neurobiology of Learning and Memory
(1998) · Elsevier eBooks · doi:10.1016/b978-0-12-475655-7.x5000-x · Cited by 137 · see citing works
Absence of systems consolidation of fear memories after dorsal, ventral, or complete hippocampal damage
Sutherland, R. J., O'Brien, J., & Lehmann, H. (2008) · Hippocampus · doi:10.1002/hipo.20431 · Cited by 137 · see citing works
The effects of neurotoxic hippocampal lesions on two effects of context after fear extinction.
Frohardt, R. J., Guarraci, F. A., & Bouton, M. E. (2000) · Behavioral Neuroscience · doi:10.1037//0735-7044.114.2.227 · Cited by 136 · see citing works
Contributions of postrhinal and perirhinal cortex to contextual information processing.
Bucci, D. J., Phillips, R. G., & Burwell, R. D. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.5.882 · Cited by 136 · see citing works
Context- but not familiarity-dependent forms of object recognition are impaired following excitotoxic hippocampal lesions in rats.
Good, M. A., Barnes, P., Staal, V., McGregor, A., & Honey, R. C. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.1.218 · Cited by 134 · see citing works
Ibotenate lesions of the hippocampus impair spatial learning but not contextual fear conditioning in mice
Cho, Y. H., Friedman, E. L., & Silva, A. J. (1998) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00054-0 · Cited by 134 · see citing works
Complete or partial hippocampal damage produces equivalent retrograde amnesia for remote contextual fear memories
Lehmann, H., Lacanilao, S., & Sutherland, R. J. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05374.x · Cited by 129 · see citing works
Dendritic properties of hippocampal CA1 pyramidal neurons in the rat: Intracellular staining in vivo and in vitro
Pyapali, G. K., Attila Gabor, S. I. K., Penttonen, M., Buzsáki, G., & Turner, D. A. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980216)391:3 · Cited by 128 · see citing works
Neurotoxic or electrolytic lesions of the ventral subiculum produce deficits in the acquisition and expression of Pavlovian fear conditioning in rats.
Maren, S. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.2.283 · Cited by 127 · see citing works
A Search for Context-Stimulus Associations in Latent Inhibition
Hall, G., & Minor, H. (1984) · The Quarterly Journal of Experimental Psychology Section B · doi:10.1080/14640748408402200 · Cited by 125 · see citing works
Extension of a New Two-Trial Memory Task in the Rat: Influence of Environmental Context on Recognition Processes
Dellu-Hagedorn, F., Fauchey, V., Moal, M. L., & Simon, H. (1997) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1997.3746 · Cited by 124 · see citing works
Disruptive effects of posttraining perirhinal cortex lesions on conditioned fear: Contributions of contextual cues.
Corodimas, K. P., & LeDoux, J. E. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.4.613 · Cited by 119 · see citing works
The role of the rat hippocampal system in several effects of context in extinction.
Wilson, A., Brooks, D. C., & Bouton, M. E. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.5.828 · Cited by 115 · see citing works
The effects of neurotoxic hippocampal lesions on two effects of context after fear extinction.
Frohardt, R. J., Guarraci, F. A., & Bouton, M. E. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.2.227 · Cited by 114 · see citing works
Contributions of the retrosplenial and posterior parietal cortices to cue-specific and contextual fear conditioning.
Keene, C. S., & Bucci, D. J. (2008) · Behavioral Neuroscience · doi:10.1037/0735-7044.122.1.89 · Cited by 113 · see citing works
Contextual fear discrimination is impaired by damage to the postrhinal or perirhinal cortex
Bucci, D. J., Saddoris, M. P., & Burwell, R. D. (2002) · Behavioral Neuroscience · doi:10.1037/0735-7044.116.3.479 · Cited by 109 · see citing works
Environmental control of defensive reactions to footshock
Blanchard, R. J., Fukunaga, K. K., & Blanchard, D. C. (1976) · Bulletin of the Psychonomic Society · doi:10.3758/bf03335103 · Cited by 106 · see citing works
Inhibitory Interconnections Control Burst Pattern and Emergent Network Synchrony in Reticular Thalamus
Sohal, V. S., & Huguenard, J. R. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-26-08978.2003 · Cited by 97 · see citing works
Hippocampal and extrahippocampal systems compete for control of contextual fear: Role of ventral subiculum and amygdalaPreprint
Biedenkapp, J. C., & Rudy, J. W. (2008) · Learning & Memory · doi:10.1101/lm.1099109 · Cited by 89 · see citing works
Self-citation
Making context memories independent of the hippocampusPreprint
Lehmann, H., Sparks, F. T., Spanswick, S. C., Hadikin, C., McDonald, R. J., & Sutherland, R. J. (2009) · Learning & Memory · doi:10.1101/lm.1385409 · Cited by 86 · see citing works
Macrophage and microglia-like cells in the avian inner ear
Bhave, S. A., Oesterle, E. C., & Coltrera, M. D. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980824)398:2 · Cited by 77 · see citing works
The Hippocampus and Context Revisited
Nadel, L. (2008) · Hippocampal Place Fields · doi:10.1093/acprof:oso/9780195323245.003.0002 · Cited by 74 · see citing works
Contingent versus incidental context processing during conditioning: Dissociation after excitotoxic hippocampal plus dentate gyrus lesions
Good, M. A., de Hoz, L., & Morris, R. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1998)8:2 · Cited by 67 · see citing works
The Hippocampal System and Declarative Memory in Humans and Animals: Experimental Analysis and Historical Origins
(1994) · The MIT Press eBooks · doi:10.7551/mitpress/4545.003.0007 · Cited by 67 · see citing works
Acquired equivalence and distinctiveness of cues: II. Neural manipulations and their implications.
Coutureau, É., Killcross, S., Good, M. A., Marshall, V. J., Ward-Robinson, J., & Honey, R. C. (2002) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.28.4.388 · Cited by 65 · see citing works
Retrograde amnesia for visual memories after hippocampal damage in ratsPreprint
Epp, J. R., Keith, J. R., Spanswick, S. C., Stone, J. C., Prusky, G. T., & Sutherland, R. J. (2008) · Learning & Memory · doi:10.1101/lm.788008 · Cited by 63 · see citing works
NMDA Receptor Modulation of Incidental Learning in Pavlovian Context Conditioning.
Stote, D. L., & Fanselow, M. S. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.1.253 · Cited by 54 · see citing works
Effects of the interval between exposure to a novel environment and the occurrence of shock on the freezing responses of rats.
Westbrook, R. F., Good, A. J., & Kiernan, M. J. (1994) · PubMed · Cited by 52 · see citing works
Entorhinal cortex lesions disrupt fear conditioning to background context but spare fear conditioning to a tone in the rat
Majchrzak, M. J., Ferry, B., Marchand, A. R., Herbeaux, K., Seillier, A., & Barbelivien, A. (2005) · Hippocampus · doi:10.1002/hipo.20138 · Cited by 50 · see citing works
Effects of lesions to the hippocampus or the fornix on allocentric conditional associative learning in rats
Sziklas, V., & Petrides, M. (2002) · Hippocampus · doi:10.1002/hipo.10030 · Cited by 39 · see citing works
The temporal dynamics of retention of a context memory: Something is missingPreprint
Rudy, J. W., & Wright-Hardesty, K. J. (2005) · Learning & Memory · doi:10.1101/lm.84005 · Cited by 32 · see citing works
Self-citation
Cue-context interactions in discrimination, categorization, and memory
Medin, D. L., & Reynolds, T. J. (1985) · Cited by 25 · see citing works
Conditioned suppression tests of the context-blocking hypothesis: Testing in the absence of the preconditioned context.
Ayres, J. J. B., Bombace, J. C., Shurtleff, D., & Vigorito, M. (1985) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037//0097-7403.11.1.1 · Cited by 24 · see citing works
Functional dissociation between fornix and hippocampus in spatial conditional learning
Dumont, J. R., Petrides, M., & Sziklas, V. (2007) · Hippocampus · doi:10.1002/hipo.20353 · Cited by 18 · see citing works
Conditioned suppression tests of the context-blocking hypothesis: Testing in the absence of the preconditioned context.
Ayres, J. J. B., Bombace, J. C., Shurtleff, D., et al. (1985) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.11.1.1 · Cited by 18 · see citing works
Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways.
Lavenex (2000) · Pure Amsterdam UMC · doi:10.1002/1098-1063(2000)10:4 · Cited by 1 · see citing works
Untitled work
(1997) · doi:10.1002/(sici)1098-1063(1997)7:4

Flagged first, then by citations

Research works printed but not linked: 3

Nadel L, Willner J, Kurz EM. 1985. Cognitive maps and environmental context. In Context and learning (eds. P Balsam and A Tomie), pp. 385-406. Erlbaum, Hillsdale, NJ.
Randich A, Ross RT. 1985. Contextual stimuli mediate the effects of pre-and post-exposure to the unconditioned stimulus on condition suppress. In Context and learning (eds. PD Balsam and A Tomie), pp. 105-132.
Thomas DR. 1985. Contextual stimulus control of operant responding in pigeons. In Context and learning (eds. PD Balsam and A Tomie), pp. 295-322. Erlbaum, Hillsdale, NJ.

Sorted by citations

The contextual brain: implications for fear conditioning, extinction and psychopathology
Maren, S., Phan, K. L., & Liberzon, I. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3492 · Cited by 1,547 · see citing works
Don’t fear “fear conditioning”: Methodological considerations for the design and analysis of studies on human fear acquisition, extinction, and return of fear
Lonsdorf, T. B., Menz, M. M., Andreatta, M., Fullana, M. A., Golkar, A., Haaker, J., Heitland, I., Hermann, A., Kuhn, M., Kruse, O., et al. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.02.026 · Cited by 837 · see citing works
Fear Extinction and Relapse: State of the Art
Vervliet, B., Craske, M. G., & Hermans, D. (2013) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-050212-185542 · Cited by 671 · see citing works
The neurobiology of depression and antidepressant action
Willner, P., Scheel-Krüger, J., & Belzung, C. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.12.007 · Cited by 519 · see citing works
Memory formation and long-term retention in humans and animals: Convergence towards a transformation account of hippocampal–neocortical interactions
Winocur, G., Moscovitch, M., & Bontempi, B. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.04.016 · Cited by 486 · see citing works
A systematic review and meta-analysis of magnetic resonance imaging measurement of structural volumes in posttraumatic stress disorder
O'Doherty, D. C. M., Chitty, K. M., Saddiqui, S., Bennett, M. R., & Lagopoulos, J. (2015) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2015.01.002 · Cited by 375 · see citing works
The rodent hippocampus is essential for nonspatial object memory
Cohen, S. J., Munchow, A. H., Rios, L. M., Zhang, G., Ásgeirsdóttir, H. N., & Stackman, R. W. (2013) · Current Biology · doi:10.1016/j.cub.2013.07.002 · Cited by 325 · see citing works
Adolescent neurobiological susceptibility to social context
Schriber, R. A., & Guyer, A. E. (2016) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.12.009 · Cited by 246 · see citing works
From contextual fear to a dynamic view of memory systems
Fanselow, M. S. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2009.10.008 · Cited by 227 · see citing works
Scene Construction, Visual Foraging, and Active Inference
Mirza, M. B., Adams, R. A., Mathys, C. D., & Friston, K. J. (2016) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2016.00056 · Cited by 165 · see citing works
Orexins and fear: Implications for the treatment of anxiety disorders
Flores, Á., Saravia, R., Maldonado, R., & Berrendero, F. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.06.005 · Cited by 102 · see citing works
Long-term expression of human contextual fear and extinction memories involves amygdala, hippocampus and ventromedial prefrontal cortex: a reinstatement study in two independent samples
Lonsdorf, T. B., Haaker, J., & Kalisch, R. (2014) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsu018 · Cited by 89 · see citing works
Epigenetic mechanisms in fear conditioning: Implications for treating post-traumatic stress disorder
Kwapis, J. L., & Wood, M. A. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.08.005 · Cited by 87 · see citing works
Reduced hippocampal volume is associated with overgeneralization of negative context in individuals with PTSD
Levy-Gigi, E., Szabo, C., Richter-Levin, G., & Kéri, S. (2015) · Neuropsychology · doi:10.1037/neu0000131 · Cited by 85 · see citing works
Initial and sustained brain responses to contextual conditioned anxiety in humans
Andreatta, M., Glotzbach-Schoon, E., Mühlberger, A., Schulz, S. M., Wiemer, J., & Pauli, P. (2015) · Cortex · doi:10.1016/j.cortex.2014.09.014 · Cited by 73 · see citing works
Design of a Neurally Plausible Model of Fear Learning
Krasne, F. B., Fanselow, M. S., & Zelikowsky, M. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00041 · Cited by 51 · see citing works
An investigation of the effects of hippocampal lesions in rats on pre‐ and postoperatively acquired spatial memory in a complex environment
Winocur, G., Moscovitch, M., Rosenbaum, R. S., & Sekeres, M. (2010) · Hippocampus · doi:10.1002/hipo.20721 · Cited by 49 · see citing works
Imbalanced sensitivities to primary and secondary rewards in internet gaming disorder
(2021) · Journal of Behavioral Addictions · doi:10.1556/2006.2021.00072 · Cited by 44 · see citing works
Wild, free-living hummingbirds can learn what happened, where and in which context
Jelbert, S. A., Hurly, T. A., Marshall, R. E. S., & Healy, S. D. (2014) · Animal Behaviour · doi:10.1016/j.anbehav.2013.12.028 · Cited by 25 · see citing works
A temporal context repetition effect in rats during a novel object recognition memory task
Manns, J. R., Galloway, C. R., & Sederberg, P. B. (2015) · Animal Cognition · doi:10.1007/s10071-015-0871-3 · Cited by 4 · see citing works

Entorhinal cortex of the mouse: Cytoarchitectonical organization
van Groen, T. (2001) · Hippocampus · doi:10.1002/hipo.1054 · Cited by 53 · see citing works
Entorhinal cortex of the mouse: Cytoarchitectonical organization
van Groen, T. (2001) · Hippocampus · doi:10.1002/hipo.1054.abs · Cited by 1 · see citing works
Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices
Suzuki, W., & Amaral, D. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-03-01856.1994 · Cited by 587 · see citing works
Neurons and networks in the entorhinal cortex: A reappraisal of the lateral and medial entorhinal subdivisions mediating parallel cortical pathways
Nilssen, E. S., Doan, T. P., Nigro, M. J., Ohara, S., & Witter, M. P. (2019) · Hippocampus · doi:10.1002/hipo.23145 · Cited by 178 · see citing works
The Parahippocampal Region: Corticocortical Connectivity
Burwell, R. D. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06717.x · Cited by 513 · see citing works

Authors: Rudy, J. W.
Affiliations: University of Colorado Boulder (US)
Corresponding author: Rudy, Jerry W.
ORCID: Rudy, Jerry W.
Venue: Learning & Memory
Publisher: Cold Spring Harbor Laboratory
Published: 2009-09-30
Volume: 16
Issue: 10
Pages: 573-585
ISSN: 1072-0502 (ISSN-L)
1549-5485
DOI: 10.1101/lm.1494409
PMC: PMC2769166
OpenAlex: W2151803046
Cited by: 296
References: 131
Citations by year: 2026: 10 · 2025: 12 · 2024: 16 · 2023: 12 · 2022: 12 · 2021: 13 · 2020: 14 · 2019: 26 · 2018: 16 · 2017: 23 · 2016: 22 · 2015: 22 · 2014: 26 · 2013: 27 · 2012: 17
Type: posted content
Language: en
Open access: bronze
doi.org
Locations: Learning & Memory (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Institute of Mental Health (R01 MH 61316, R01MH061316)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: context representation, hippocampal formation, dual-process theory, perirhinal cortex, postrhinal cortex, entorhinal cortex, hippocampal-dependent memory
MeSH terms: Animals, Hippocampus, Humans, Mental Processes, Parahippocampal Gyrus

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Context representations, context functions, and the parahippocampal–hippocampal system

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks