Covert rapid action-memory simulation (CRAMS): a hypothesis of hippocampal-prefrontal interactions for adaptive behavior

Wang, Jane X.; Cohen, Neal J.; Voss, Joel L.

doi:10.1016/j.nlm.2014.04.003

Cited by 75Memory and Neural MechanismsNeural and Behavioral Psychology StudiesMemory Processes and Influences

Covert rapid action-memory simulation (CRAMS): a hypothesis of hippocampal-prefrontal interactions for adaptive behavior

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Wang, Jane X., Cohen, Neal J., Voss, Joel L.·2015·Neurobiology of Learning and Memory

DOI 10.1016/j.nlm.2014.04.003PMC PMC4291298

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Abstract

Effective choices generally require memory, yet little is known regarding the cognitive or neural mechanisms that allow memory to influence choices. We outline a new framework proposing that covert memory processing of hippocampus interacts with action-generation processing of prefrontal cortex in order to arrive at optimal, memory-guided choices. Covert, rapid action-memory simulation (CRAMS) is proposed here as a framework for understanding cognitive and/or behavioral choices, whereby prefrontal-hippocampal interactions quickly provide multiple simulations of potential outcomes used to evaluate the set of possible choices. We hypothesize that this CRAMS process is automatic, obligatory, and covert, meaning that many cycles of action-memory simulation occur in response to choice conflict without an individual's necessary intention and generally without awareness of the simulations, leading to adaptive behavior with little perceived effort. CRAMS is thus distinct from influential proposals that adaptive memory-based behavior in humans requires consciously experienced memory-based construction of possible future scenarios and deliberate decisions among possible future constructions. CRAMS provides an account of why hippocampus has been shown to make critical contributions to the short-term control of behavior, and it motivates several new experimental approaches and hypotheses that could be used to better understand the ubiquitous role of prefrontal-hippocampal interactions in situations that require adaptively using memory to guide choices. Importantly, this framework provides a perspective that allows for testing decision-making mechanisms in a manner that translates well across human and nonhuman animal model systems.

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Hippocampal-prefrontal interaction has been suggested to allow rapid, subconscious evaluation of potential action sequences during decision-making, with the hippocampus simulating expected outcomes of potential actions generated and evaluated in the prefrontal.
“Hippocampal-prefrontal interaction has been suggested to allow rapid, subconscious evaluation of potential action sequences during decision-making, with the hippocampus in effect simulating the expected outcomes of potential actions that are generated and evaluated in the prefrontal (Mushiake et al., 2006; Wang et al., 2015).”
From Toward an integration of deep learning and neuroscience (2016) · cites this paper as Wang et al., 2015

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An Integrative Theory of Prefrontal Cortex Function
Miller, E. K., & Cohen, J. D. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.167 · Cited by 12,803 · see citing works
Untitled work
(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010 · see citing works
LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS
Scoville, W. B., & Milner, B. (1957) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.20.1.11 · Cited by 7,322 · see citing works
Rhythms of the Brain
Buzsáki, G. (2006) · doi:10.1093/acprof:oso/9780195301069.001.0001 · Cited by 4,873 · see citing works
Excitatory and Inhibitory Interactions in Localized Populations of Model Neurons
Wilson, H. R., & Cowan, J. D. (1972) · Biophysical Journal · doi:10.1016/s0006-3495(72)86068-5 · Cited by 3,579 · see citing works
Plans and the structure of behavior . By George A. Miller, Eugene Galanter, and Karl H. Pribram. Pp. X, 226. New York: Henry Holt and Co., Inc., 1960.
Brown, R. W. (1960) · Language · doi:10.2307/411065 · Cited by 3,525 · see citing works
Source monitoring.
Johnson, M. K., Hashtroudi, S., & Lindsay, D. S. (1993) · Psychological Bulletin · doi:10.1037/0033-2909.114.1.3 · Cited by 3,392 · see citing works
The Medial Temporal Lobe Memory System
Squire, L. R., & Zola-Morgan, S. (1991) · Science · doi:10.1126/science.1896849 · Cited by 3,282 · see citing works
Self-projection and the brain
Buckner, R. L., & Carroll, D. C. (2007) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2006.11.004 · Cited by 2,691 · see citing works
Purposive Behavior in Animals and Men
Rodhom, C., & Tolman, E. C. (1950) · The American Journal of Psychology · doi:10.2307/1418946 · Cited by 2,455 · see citing works
The Hippocampus as a Cognitive Map
Ranck, J. B. (1979) · American Journal of Psychiatry · doi:10.1176/ajp.136.10.1353 · Cited by 2,373 · see citing works
The Prefrontal Cortex: Anatomy, Physiology, and Neuropsychology of the Frontal Lobe
Fuster, J. M. (1980) · Cited by 2,367 · see citing works
Preserved Learning and Retention of Pattern-Analyzing Skill in Amnesia: Dissociation of Knowing How and Knowing That
Cohen, N. J., & Squire, L. R. (1980) · Science · doi:10.1126/science.7414331 · Cited by 2,296 · see citing works
Self-citation
The three-dimensional organization of the hippocampal formation: A review of anatomical data
Amaral, D. G., & Witter, M. P. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90424-7 · Cited by 2,180 · see citing works
The prefrontal cortex
Fuster, J. M. (1997) · Cited by 2,095 · see citing works
DEFICITS IN STRATEGY APPLICATION FOLLOWING FRONTAL LOBE DAMAGE IN MAN
SHALLICE, T., & BURGESS, P. W. (1991) · Brain · doi:10.1093/brain/114.2.727 · Cited by 2,017 · see citing works
The prefontral cortex and cognitive control
Miller, E. K. (2000) · Nature Reviews Neuroscience · doi:10.1038/35036228 · Cited by 2,016 · see citing works
Circuitry of Primate Prefrontal Cortex and Regulation of Behavior by Representational Memory
Goldman‐Rakic, P. S. (1987) · Comprehensive Physiology · doi:10.1002/cphy.cp010509 · Cited by 1,960 · see citing works
Temporal dynamics of brain activation during a working memory task
Cohen, J. D., Perlstein, W. M., Braver, T. S., Nystrom, L. E., Noll, D. C., Jonides, J., & Smith, E. E. (1997) · Nature · doi:10.1038/386604a0 · Cited by 1,876 · see citing works
Purposive Behavior in Animals and Men
Irwin, F. W. (1932) · Europe PMC (PubMed Central) · Cited by 1,867 · see citing works
The cognitive neuroscience of constructive memory: remembering the past and imagining the future
Schacter, D. L., & Addis, D. R. (2007) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2007.2087 · Cited by 1,836 · 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
Neural Mechanisms of Visual Working Memory in Prefrontal Cortex of the Macaque
Miller, E. K., Erickson, C. A., & Desimone, R. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-16-05154.1996 · Cited by 1,441 · see citing works
The future of memory: remembering, imagining, and the brain
Schacter, D. L., Addis, D. R., Hassabis, D., Martin, V. C., Spreng, R. N., & Szpunar, K. K. (2012) · Neuron · doi:10.1016/j.neuron.2012.11.001 · Cited by 1,398 · see citing works
Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat
Hoover, W. B., & Vertes, R. P. (2007) · Brain Structure and Function · doi:10.1007/s00429-007-0150-4 · Cited by 1,365 · see citing works
The hippocampus and memory: insights from spatial processing
Bird, C. M., & Burgess, N. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2335 · Cited by 1,313 · see citing works
Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach
Norman, K. A., & O'Reilly, R. C. (2003) · Psychological Review · doi:10.1037/0033-295x.110.4.611 · Cited by 1,312 · see citing works
Hippocampal place-cell sequences depict future paths to remembered goals
Pfeiffer, B. E., & Foster, D. J. (2013) · Nature · doi:10.1038/nature12112 · Cited by 1,216 · see citing works
Single neurons in prefrontal cortex encode abstract rules
Wallis, J. D., Anderson, K. C., & Miller, E. K. (2001) · Nature · doi:10.1038/35082081 · Cited by 1,075 · see citing works
From Conditioning to Conscious Recollection
Eichenbaum, H., & Cohen, N. J. (2004) · doi:10.1093/acprof:oso/9780195178043.001.0001 · Cited by 1,026 · see citing works
Self-citation
Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point
Johnson, A., & Redish, A. D. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3761-07.2007 · Cited by 1,003 · see citing works
Medial prefrontal cortex as an action-outcome predictor
Alexander, W. H., & Brown, J. W. (2011) · Nature Neuroscience · doi:10.1038/nn.2921 · Cited by 1,000 · see citing works
Prefrontal and medial temporal lobe interactions in long-term memory
Simons, J. S., & Spiers, H. J. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1178 · Cited by 961 · see citing works
Is the rostro-caudal axis of the frontal lobe hierarchical?
Badre, D., & D'Esposito, M. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2667 · Cited by 946 · see citing works
State-dependent computations: spatiotemporal processing in cortical networks
Buonomano, D. V., & Maass, W. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2558 · Cited by 919 · see citing works
An adaptive coding model of neural function in prefrontal cortex
Duncan, J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35097575 · Cited by 874 · see citing works
Coherent theta oscillations and reorganization of spike timing in the hippocampal- prefrontal network upon learning
Benchenane, K., Peyrache, A., Khamassi, M., Tierney, P. L., Gioanni, Y., Battaglia, F. P., & Wiener, S. I. (2010) · Neuron · doi:10.1016/j.neuron.2010.05.013 · Cited by 872 · see citing works
Choice, uncertainty and value in prefrontal and cingulate cortex
Rushworth, M. F. S., & Behrens, T. E. J. (2008) · Nature Neuroscience · doi:10.1038/nn2066 · Cited by 866 · see citing works
Episodic Simulation of Future Events: Concepts, Data, and Applications
Schacter, D. L., Addis, D. R., & Buckner, R. L. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1440.001 · Cited by 840 · see citing works
The entorhinal cortex of the monkey: II. Cortical afferents
Insausti, R., Amaral, D. G., & Cowan, W. M. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902640306 · Cited by 835 · see citing works
Awake replay of remote experiences in the hippocampus
Karlsson, M. P., & Frank, L. M. (2009) · Nature Neuroscience · doi:10.1038/nn.2344 · Cited by 769 · cited 1× · see citing works
“Further, awake replay of previous experiences have been found in the rat hippocampus during quiet waking states (Karlsson & Frank, 2009), in the absence of overt environmental input (but possibly due to internally generated action cues from PFC).”
Background
Amnesia and the distinction between long- and short-term memory
Baddeley, A., & Warrington, E. K. (1970) · Journal of Verbal Learning and Verbal Behavior · doi:10.1016/s0022-5371(70)80048-2 · Cited by 739 · see citing works
Human prefrontal cortex: processing and representational perspectives
Wood, J. N., & Grafman, J. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1033 · Cited by 721 · see citing works
Dynamic Coding for Cognitive Control in Prefrontal Cortex
Stokes, M. G., Kusunoki, M., Sigala, N., Nili, H., Gaffan, D., & Duncan, J. (2013) · Neuron · doi:10.1016/j.neuron.2013.01.039 · Cited by 711 · see citing works
Neurocomputational models of working memory
Durstewitz, D., Seamans, J. K., & B, T. J. S. A. (2000) · Nature Neuroscience · doi:10.1038/81460 · Cited by 710 · see citing works
Associative memory and the medial temporal lobes
Mayes, A. R., Montaldi, D., & Migo, E. M. (2007) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2006.12.003 · Cited by 681 · see citing works
Decision Making in Recurrent Neuronal Circuits
Wang, X.-J. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.034 · Cited by 679 · cited 1× · see citing works
“In general, synaptic facilitation of both afferent pathways and recurrent intra-network circuits likely affect the evolution of PFC networks toward attractor states in the absence of sensory stimulation (Wang, 2008) in a process of cognitive search (Kurth-Nelson et al., 2012).”
Background
Attention Samples Stimuli Rhythmically
Landau, A. N., & Fries, P. (2012) · Current Biology · doi:10.1016/j.cub.2012.03.054 · Cited by 612 · see citing works
Neural Activity in the Primate Prefrontal Cortex during Associative Learning
Asaad, W. F., Rainer, G., & Miller, E. K. (1998) · Neuron · doi:10.1016/s0896-6273(00)80658-3 · Cited by 593 · see citing works
The determiners of behavior at a choice point.
Tolman, E. C. (1938) · Psychological Review · doi:10.1037/h0062733 · Cited by 543 · see citing works
Task-Specific Neural Activity in the Primate Prefrontal Cortex
Asaad, W. F., Rainer, G., & Miller, E. K. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.84.1.451 · Cited by 524 · see citing works
Cortico–basal ganglia circuit mechanism for a decision threshold in reaction time tasks
Lo, C.-C., & Wang, X.-J. (2006) · Nature Neuroscience · doi:10.1038/nn1722 · Cited by 505 · see citing works
Preference by Association: How Memory Mechanisms in the Hippocampus Bias Decisions
Wimmer, G. E., & Daphna Shohamy, A. (2012) · Science · doi:10.1126/science.1223252 · Cited by 497 · see citing works
Role of the lateral prefrontal cortex in executive behavioral control.
Tanji, J., & Hoshi, E. (2008) · Physiological Reviews · doi:10.1152/physrev.00014.2007 · Cited by 495 · see citing works
The construction system of the brain
Hassabis, D., & Maguire, E. A. (2009) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2008.0296 · Cited by 483 · see citing works
Forward frontal fields: phylogeny and fundamental function
Wise, S. P. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.08.008 · Cited by 478 · cited 1× · see citing works
“That is, ventromedial PFC is densely interconnected with the rostral anterior cingulate area (Brodmann Area 32) that is the hypothesized homologue of rodent prelimibic cortex (Wise, 2008).”
Background
Primate analogue of the Wisconsin card sorting test: Effects of excitotoxic lesions of the prefrontal cortex in the marmoset.
Dias, R. S., Robbins, T. W., & Roberts, A. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.5.872 · Cited by 476 · see citing works
Primate analogue of the Wisconsin Card Sorting Test: effects of excitotoxic lesions of the prefrontal cortex in the marmoset
Dias, R., Robbins, T. W., & Roberts, A. C. (1996) · Behavioral Neuroscience · doi:10.1037/0735-7044.110.5.872 · Cited by 476 · see citing works
A map of visual space in the primate entorhinal cortex
Killian, N. J., Jutras, M. J., & Buffalo, E. A. (2012) · Nature · doi:10.1038/nature11587 · Cited by 471 · see citing works
Selection, Integration, and Conflict Monitoring
Badre, D., & Wagner, A. D. (2004) · Neuron · doi:10.1016/s0896-6273(03)00851-1 · Cited by 463 · see citing works
Frontal lobes and the temporal organization of memory.
Milner, B. A., Petrides, M., & Ml, S. (1985) · PubMed · Cited by 458 · see citing works
Specialized systems for the processing of mnemonic information within the primate frontal cortex
Petrides, M. (1996) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1996.0130 · Cited by 443 · see citing works
The Long and the Short of It: Relational Memory Impairments in Amnesia, Even at Short Lags
Hannula, D. E., Tranel, D., & Cohen, N. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5222-05.2006 · Cited by 436 · see citing works
Self-citation
Prospective coding for objects in primate prefrontal cortex
Rainer, G., Rao, S. C., & Miller, E. K. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-13-05493.1999 · Cited by 432 · see citing works
Shaping of Object Representations in the Human Medial Temporal Lobe Based on Temporal Regularities
Schapiro, A. C., Kustner, L. V., & Turk-Browne, N. B. (2012) · Current Biology · doi:10.1016/j.cub.2012.06.056 · Cited by 430 · see citing works
Rule-dependent neuronal activity in the prefrontal cortex
White, I. M., & Wise, S. P. (1999) · Experimental Brain Research · doi:10.1007/s002210050740 · Cited by 429 · see citing works
Neuroanatomy (Text and Atlas)
Hlavin, L. (1990) · Neurology · doi:10.1212/wnl.40.2.388-c · Cited by 426 · see citing works
The Role of the Hippocampus in Prediction and Imagination
Buckner, R. L. (2010) · Annual Review of Psychology · doi:10.1146/annurev.psych.60.110707.163508 · Cited by 419 · see citing works
Inactivation of Parietal and Prefrontal Cortex Reveals Interdependence of Neural Activity During Memory-Guided Saccades
Chafee, M. V., & Goldman, P. S. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.3.1550 · Cited by 406 · see citing works
Medial Temporal Lobe Activity Associated with Active Maintenance of Novel Information
Charan Ranganath, A., & D’Esposito, M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00411-1 · Cited by 391 · see citing works
A unified framework for the functional organization of the medial temporal lobes and the phenomenology of episodic memory
Ranganath, C. (2010) · Hippocampus · doi:10.1002/hipo.20852 · Cited by 375 · see citing works
An analysis of rat prefrontal cortex in mediating executive function
Kesner, R. P., & Churchwell, J. C. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.07.002 · Cited by 365 · see citing works
Implicit Perceptual Anticipation Triggered by Statistical Learning
Turk‐Browne, N. B., Scholl, B. J., Johnson, M. K., & Chun, M. M. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0858-10.2010 · Cited by 360 · see citing works
Unconscious Activation of the Cognitive Control System in the Human Prefrontal Cortex
Lau, H. C., & Passingham, R. E. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4335-06.2007 · Cited by 358 · see citing works
The Eyes Have It: Hippocampal Activity Predicts Expression of Memory in Eye Movements
Hannula, D. E., & Ranganath, C. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.025 · Cited by 352 · see citing works
Encyclopedia of Neuroscience
Simner, J. (2009) · Cited by 336 · see citing works
Relational memory and the hippocampus: Representations and methods
Konkel, A. (2009) · Frontiers in Neuroscience · doi:10.3389/neuro.01.023.2009 · Cited by 333 · see citing works
Animal Foraging and the Evolution of Goal‐Directed Cognition
Hills, T. T. (2006) · Cognitive Science · doi:10.1207/s15516709cog0000_50 · Cited by 331 · see citing works
The hippocampus supports high-resolution binding in the service of perception, working memory and long-term memory
Yonelinas, A. P. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.05.030 · Cited by 328 · see citing works
The hippocampus supports multiple cognitive processes through relational binding and comparison
Olsen, R. K., Moses, S. N., Riggs, L., & Ryan, J. D. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00146 · Cited by 306 · see citing works
Neuroanatomy: Text and Atlas
Martin, J. H. (1989) · Cited by 295 · see citing works
The Hippocampus and Imagining the Future: Where Do We Stand?
Addis, D. R., & Schacter, D. L. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2011.00173 · Cited by 285 · see citing works
Unconscious Activation of the Prefrontal No-Go Network
van Gaal, S., Ridderinkhof, K. R., Scholte, H. S., & Lamme, V. A. F. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2992-09.2010 · Cited by 276 · see citing works
Oscillatory activity in the monkey hippocampus during visual exploration and memory formation
Jutras, M. J., Fries, P., & Buffalo, E. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1302351110 · Cited by 274 · see citing works
The hippocampus and inferential reasoning: building memories to navigate future decisions
Zeithamova, D., Schlichting, M. L., & Preston, A. R. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00070 · Cited by 266 · see citing works
Subicular Input from Temporal Cortex in the Rhesus Monkey
Hoesen, G. W. V., Rosene, D. L., & Mesulam, M. M. (1979) · Science · doi:10.1126/science.109926 · Cited by 264 · see citing works
Considerations arising from a complementary learning systems perspective on hippocampus and neocortex
McClelland, J. L., & Goddard, N. (1996) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:6 · Cited by 262 · see citing works
Sensory signals during active versus passive movement
Cullen, K. E. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.10.002 · Cited by 262 · see citing works
Activity in the lateral prefrontal cortex reflects multiple steps of future events in action plans
Mushiake, H., Saito, N., Sakamoto, K., Itoyama, Y., & Tanji, J. (2006) · Neuron · doi:10.1016/j.neuron.2006.03.045 · Cited by 249 · see citing works
Bidirectional changes to hippocampal theta-gamma comodulation predict memory for recent spatial episodes
Shirvalkar, P. R., Rapp, P. R., & Shapiro, M. L. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911184107 · Cited by 235 · see citing works
Predictive, interactive multiple memory systems
Henson, R. N., & Gagnepain, P. (2010) · Hippocampus · doi:10.1002/hipo.20857 · Cited by 226 · see citing works
Behavioral planning in the prefrontal cortex
Tanji, J., & Hoshi, E. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00192-6 · Cited by 224 · see citing works
Frontopolar cortex mediates abstract integration in analogy
Green, A. E., Fugelsang, J. A., Kraemer, D. J. M., Shamosh, N. A., & Dunbar, K. N. (2006) · Brain Research · doi:10.1016/j.brainres.2006.04.024 · Cited by 216 · see citing works
Rapid Onset Relational Memory Effects Are Evident in Eye Movement Behavior, but Not in Hippocampal Amnesia
Hannula, D. E., Ryan, J. D., Tranel, D., & Cohen, N. J. (2007) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2007.19.10.1690 · Cited by 215 · see citing works
Self-citation
On the Neural Correlates of Visual Perception
Pollen, D. A. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.1.4 · Cited by 213 · see citing works
Hippocampal Amnesia Impairs All Manner of Relational Memory
Konkel, A. (2008) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.015.2008 · Cited by 213 · see citing works
Prediction of vicarious trial and error by means of the schematic sowbug.
Tolman, E. C. (1939) · Psychological Review · doi:10.1037/h0057054 · Cited by 206 · see citing works
Role of the hippocampus in remembering the past and imagining the future
Squire, L. R., van der Horst, A. S., McDuff, S. G. R., Frascino, J. C., Hopkins, R. O., & Mauldin, K. N. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1014391107 · Cited by 206 · see citing works
Hippocampal brain-network coordination during volitional exploratory behavior enhances learning
Voss, J. L., Gonsalves, B. D., Federmeier, K. D., Tranel, D., & Cohen, N. J. (2010) · Nature Neuroscience · doi:10.1038/nn.2693 · Cited by 203 · see citing works
Self-citation
Excitatory amino acid pathway from the hippocampus to the prefrontal cortex. Contribution of AMPA receptors in hippocampo-prefrontal cortex transmission
Jay, T. M., Thierry, A., Wiklund, L., & Glowinski, J. (1992) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1992.tb00154.x · Cited by 187 · see citing works
Information Processing in Decision-Making Systems
van der Meer, M. A. A., Kurth-Nelson, Z. L., & Redish, A. D. (2012) · The Neuroscientist · doi:10.1177/1073858411435128 · Cited by 186 · see citing works
Coupled oscillations mediate directed interactions between prefrontal cortex and hippocampus of the neonatal rat
Brockmann, M. D., Pöschel, B., Cichon, N., & Hanganu-Opatz, I. L. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.041 · Cited by 186 · see citing works
Item and order dissociation in humans with prefrontal cortex damage
Kesner, R. P., Hopkins, R. O., & Fineman, B. (1994) · Neuropsychologia · doi:10.1016/0028-3932(94)90040-x · Cited by 179 · see citing works
Vicarious Trial and Error at a Point of Choice: I. A General Survey of its Relation to Learning Efficiency
Muenzinger, K. F. (1938) · The Pedagogical Seminary and Journal of Genetic Psychology · doi:10.1080/08856559.1938.10533799 · Cited by 178 · see citing works
Top–Down Attentional Deficits in Macaques with Lesions of Lateral Prefrontal Cortex
Rossi, A. F., Bichot, N. P., Desimone, R., & Ungerleider, L. G. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2939-07.2007 · Cited by 173 · see citing works
The contribution of distinct subregions of the ventromedial frontal cortex to emotion, social behavior, and decision making
Rudebeck, P. H., Bannerman, D. M., & Rushworth, M. F. S. (2008) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.8.4.485 · Cited by 172 · see citing works
The Dynamic Nature of Top-Down Signals Originating from Prefrontal Cortex: A Combined fMRI–TMS Study
Lee, T. G., & D’Esposito, M. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0627-12.2012 · Cited by 161 · see citing works
Search in External and Internal Spaces
Hills, T. T., Todd, P. M., & Goldstone, R. L. (2008) · Psychological Science · doi:10.1111/j.1467-9280.2008.02160.x · Cited by 157 · see citing works
Identification of the Hippocampal Input to Medial Prefrontal Cortex In Vitro
Parent, M. A., Wang, L., Su, J., Netoff, T. I., & Yuan, L. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp108 · Cited by 149 · see citing works
Memory and the Prefrontal Cortexa
Shimamura, A. P. (1995) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1995.tb38136.x · Cited by 136 · see citing works
The hippocampus reevaluated in unconscious learning and memory: at a tipping point?
Hannula, D. E., & Greene, A. J. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00080 · Cited by 133 · see citing works
Cortical efferents of the entorhinal cortex and the adjacent parahippocampal region in the monkey ( Macaca fascicularis )
Muñoz, M., & Insausti, R. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04299.x · Cited by 127 · see citing works
Complimentary roles for hippocampal versus subicular/entorhinal place cells in coding place, context, and events
Sharp, P. E. (1999) · Hippocampus · doi:10.1002/(sici)1098-1063(1999)9:4 · Cited by 125 · see citing works
The central executive as a search process: Priming exploration and exploitation across domains.
Hills, T. T., Todd, P. M., & Goldstone, R. L. (2010) · Journal of Experimental Psychology General · doi:10.1037/a0020666 · Cited by 125 · see citing works
Spatial reconstruction by patients with hippocampal damage is dominated by relational memory errors
Watson, P. D., Voss, J. L., Warren, D. E., Tranel, D., & Cohen, N. J. (2013) · Hippocampus · doi:10.1002/hipo.22115 · Cited by 123 · see citing works
Self-citation
Spontaneous revisitation during visual exploration as a link among strategic behavior, learning, and the hippocampus
Voss, J. L., Warren, D. E., Gonsalves, B. D., Federmeier, K. D., Tranel, D., & Cohen, N. J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100225108 · Cited by 122 · see citing works
Self-citation
Representation of Immediate and Final Behavioral Goals in the Monkey Prefrontal Cortex during an Instructed Delay Period
Saito, N., Mushiake, H., Sakamoto, K., Itoyama, Y., & Tanji, J. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi032 · Cited by 121 · see citing works
A simple test of the vicarious trial-and-error hypothesis of hippocampal function.
Hu, D., & Amsel, A. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.12.5506 · Cited by 119 · see citing works
Area-Selective Neuronal Activity in the Dorsolateral Prefrontal Cortex for Information Retrieval and Action Planning
Hoshi, E., & Tanji, J. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00904.2003 · Cited by 115 · see citing works
Long-term potentiation of hippocampal afferents and efferents to prefrontal cortex: Implications for associative learning
Doyère, V., Burette, F., Negro, C. D., & Laroche, S. (1993) · Neuropsychologia · doi:10.1016/0028-3932(93)90031-t · Cited by 112 · see citing works
Connectivity-based parcellation of the human frontal pole with diffusion tensor imaging
Liu, H., Qin, W., Li, W., Fan, L., Wang, J., Jiang, T., & Yu, C. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.4882-12.2013 · Cited by 108 · see citing works
Self-citation
Imagining fictitious and future experiences: Evidence from developmental amnesia
Maguire, E. A., Vargha‐Khadem, F., & Hassabis, D. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.06.037 · Cited by 99 · see citing works
The neurobiology of memory based predictions
Eichenbaum, H., & Fortin, N. J. (2009) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0306 · Cited by 99 · see citing works
A theoretical account of cognitive effects in delay discounting
Kurth-Nelson, Z. L., Bickel, W. K., & Redish, A. D. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08058.x · Cited by 97 · see citing works
Losing sight of the future: Impaired semantic prospection following medial temporal lobe lesions
Race, E., Keane, M. M., & Verfaellie, M. H. (2012) · Hippocampus · doi:10.1002/hipo.22084 · Cited by 87 · see citing works
Mechanisms of Rule Acquisition and Rule Following in Inductive Reasoning
Crescentini, C., Seyed‐Allaei, S., Pisapia, N. D., Jovicich, J., Amati, D., & Shallice, T. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4579-10.2011 · Cited by 81 · see citing works
Synchronization of Medial Temporal Lobe and Prefrontal Rhythms in Human Decision Making
Guitart‐Masip, M., Barnes, G. R., Horner, A. J., Bauer, M., Dolan, R. J., & Düzel, E. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2573-12.2013 · Cited by 79 · see citing works
The role of the hippocampus in retaining relational information across short delays: The importance of memory loadPreprint
Jeneson, A., Mauldin, K. N., Hopkins, R. O., & Squire, L. R. (2011) · Learning & Memory · doi:10.1101/lm.2010711 · Cited by 70 · see citing works
Effects on executive function following damage to the prefrontal cortex in the rhesus monkey (Macaca mulatta).
Moore, T. L., Schettler, S. P., Killiany, R., Rosene, D. L., & Moss, M. B. (2009) · Behavioral Neuroscience · doi:10.1037/a0014723 · Cited by 65 · see citing works
The hippocampus and exploration: dynamically evolving behavior and neural representations
Johnson, A., Varberg, Z., Benhardus, J., Maahs, A., & Schrater, P. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00216 · Cited by 61 · see citing works
Sustained neural activity associated with cognitive control during temporally extended decision making
Yarkoni, T., Gray, J. R., Chrastil, E. R., Barch, D. M., Green, L., & Braver, T. S. (2005) · Cognitive Brain Research · doi:10.1016/j.cogbrainres.2005.01.013 · Cited by 59 · see citing works
Role of active movement in place-specific firing of hippocampal neurons
Song, E. Y., Kim, Y. B., Kim, Y. H., & Jung, M. W. (2004) · Hippocampus · doi:10.1002/hipo.20023 · Cited by 57 · see citing works
Reward-Related Learning via Multiple Memory Systems
Delgado, M. R., & Dickerson, K. C. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.01.023 · Cited by 55 · see citing works
Medial temporal lobe damage impairs representation of simple stimuli
Warren, D. E. (2010) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2010.00035 · Cited by 53 · see citing works
The hippocampus uses information just encountered to guide efficient ongoing behavior
Yee, L. T. S., Warren, D. E., Voss, J. L., Duff, M. C., Tranel, D., & Cohen, N. J. (2013) · Hippocampus · doi:10.1002/hipo.22211 · Cited by 40 · see citing works
Self-citation
People's study time allocation and its relation to animal foraging
Metcalfe, J., & Jacobs, W. J. (2009) · Behavioural Processes · doi:10.1016/j.beproc.2009.12.011 · Cited by 38 · see citing works
PREFRONTAL BRAIN ACTIVITY PREDICTS TEMPORALLY EXTENDED DECISION-MAKING BEHAVIOR
Yarkoni, T., Braver, T. S., Gray, J. R., & Green, L. (2005) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.2005.121-04 · Cited by 38 · see citing works
The neural substrates of deliberative decision making: contrasting effects of hippocampus lesions on performance and vicarious trial-and-error behavior in a spatial memory task and a visual discrimination task
Bett, D., Allison, E. K., Murdoch, L. H., Kaefer, K., Wood, E. R., & Dudchenko, P. A. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00070 · Cited by 36 · see citing works
Chapter 1 Involvement of the Prefrontal Cortex in Problem Solving
Mushiake, H., Sakamoto, K., Saito, N., Inui, T., Aihara, K., & Tanji, J. (2009) · International review of neurobiology · doi:10.1016/s0074-7742(09)85001-0 · Cited by 27 · see citing works
The basal ganglia, the ideal machinery for the cost-benefit analysis of action plans
Hwang, E. J. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00121 · Cited by 23 · see citing works
Strategic Control of Memory
Kuhl, B. A., & Wagner, A. D. (2009) · Elsevier eBooks · doi:10.1016/b978-008045046-9.00424-1 · Cited by 18 · see citing works

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Fuster JM 1995 Memory in the cerebal cortex Cambridge MIT Press
Fuster JM 2008 The prefrontal cortex Amsterdam Elsevier

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The role of the hippocampus in flexible cognition and social behavior
Rubin, R. D., Watson, P. D., Duff, M. C., & Cohen, N. J. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00742 · Cited by 489 · see citing works
Self-citation
Differential contributions of hippocampus and medial prefrontal cortex to self-projection and self-referential processing
Kurczek, J., Wechsler, E., Ahuja, S., Jensen, U., Cohen, N. J., Tranel, D., & Duff, M. (2015) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2015.05.002 · Cited by 157 · see citing works
Self-citation
Toward an integration of deep learning and neuroscience
Marblestone, A. H., Wayne, G., & Kording, K. P. (2016) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2016.00094 · Cited by 119 · see citing works
Chemerin-9 Peptide Enhances Memory and Ameliorates Aβ1–42-Induced Object Memory Impairment in Mice
Lei, Z., Lu, Y., Bai, X., Jiang, Z., & Yu, Q. (2020) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.b19-00510 · Cited by 23 · see citing works

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Buekens, F. (2016) · Phenomenology and Mind · doi:10.13128/phe_mi-19625 · Cited by 2 · see citing works
Covert Events: The Logical Status of First-Person Reports
Zuriff, G. E. (1979) · The Psychological Record · doi:10.1007/bf03394598 · Cited by 11 · see citing works
Chameleonizing: A microsociological study of covert physical surveillance
Dahl, J. Y. (2020) · European Journal of Criminology · doi:10.1177/1477370819896204 · Cited by 9 · see citing works
Considering covert surveillance
Tickner, P. (2012) · doi:10.1002/9781119205807.ch8
Covert interview and profssional morality of press——Also about public-convincing power
Wang, Y. (2006) · Journal of Bohai University

Authors: Wang, J. X., Cohen, N. J., & Voss, J. L.
Affiliations: Northwestern University (US)
University of Illinois Urbana-Champaign (US)
Corresponding author: Voss, Joel L.
ORCID: Wang, Jane X.
Cohen, Neal J.
Voss, Joel L.
Venue: Neurobiology of Learning and Memory
Publisher: Elsevier BV
Published: 2015-01
Volume: 117
Pages: 22-33
ISSN: 1074-7427 (ISSN-L)
DOI: 10.1016/j.nlm.2014.04.003
PMC: PMC4291298
OpenAlex: W2028706091
Cited by: 75
References: 141
Citations by year: 2025: 3 · 2024: 4 · 2023: 7 · 2022: 3 · 2021: 8 · 2020: 7 · 2019: 8 · 2018: 6 · 2017: 6 · 2016: 6 · 2015: 11 · 2014: 6
FWCI: 0.93
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neurobiology of Learning and Memory (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Neurological Disorders and Stroke
National Institute of Mental Health
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Keywords: hippocampus, prefrontal cortex, decision-making, adaptive behavior
MeSH terms: Adaptation, Psychological, Animals, Decision Making, Hippocampus, Humans, Memory, Models, Neurological, Neural Pathways, Psychomotor Performance, Prefrontal Cortex

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Covert rapid action-memory simulation (CRAMS): a hypothesis of hippocampal-prefrontal interactions for adaptive behavior

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