Decoding the Cognitive Map: Ensemble Hippocampal Sequences and Decision Making

Overview

Journal Curr Opin Neurobiol

Specialties Biology
Neurology

Date 2014 Dec 3

PMID 25463559

Citations 45

Authors

Andrew M Wikenheiser

A David Redish

Affiliations

Soon will be listed here.

Abstract

Tolman proposed that complex animal behavior is mediated by the cognitive map, an integrative learning system that allows animals to reconfigure previous experience in order to compute predictions about the future. The discovery of place cells in the rodent hippocampus immediately suggested a plausible neural mechanism to fulfill the 'map' component of Tolman's theory. Recent work examining hippocampal representations occurring at fast time scales suggests that these sequences might be important for supporting the inferential mental operations associated with the cognitive map function. New findings that hippocampal sequences play an important causal role in mediating adaptive behavior on a moment-by-moment basis suggest specific neural processes that may underlie Tolman's cognitive map framework.

Citing Articles

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Working memory features are embedded in hippocampal place fields.

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Liu C, Todorova R, Tang W, Oliva A, Fernandez-Ruiz A Science. 2023; 382(6668):eadi8237.

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References

van der Meer M, Redish A . Expectancies in decision making, reinforcement learning, and ventral striatum. Front Neurosci. 2011; 4:6. PMC: 2891485. DOI: 10.3389/neuro.01.006.2010. View

Jones M, Wilson M . Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm. Hippocampus. 2005; 15(7):867-73. DOI: 10.1002/hipo.20119. View

Hyman J, Zilli E, Paley A, Hasselmo M . Working Memory Performance Correlates with Prefrontal-Hippocampal Theta Interactions but not with Prefrontal Neuron Firing Rates. Front Integr Neurosci. 2010; 4:2. PMC: 2861479. DOI: 10.3389/neuro.07.002.2010. View

Gupta A, van der Meer M, Touretzky D, Redish A . Hippocampal replay is not a simple function of experience. Neuron. 2010; 65(5):695-705. PMC: 4460981. DOI: 10.1016/j.neuron.2010.01.034. View

Pavlides C, WINSON J . Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J Neurosci. 1989; 9(8):2907-18. PMC: 6569689. View

Vanderwolf C . Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol. 1969; 26(4):407-18. DOI: 10.1016/0013-4694(69)90092-3. View

Amemiya S, Noji T, Kubota N, Nishijima T, Kita I . Noradrenergic modulation of vicarious trial-and-error behavior during a spatial decision-making task in rats. Neuroscience. 2014; 265:291-301. DOI: 10.1016/j.neuroscience.2014.01.031. View

Lansink C, Goltstein P, Lankelma J, Joosten R, McNaughton B, Pennartz C . Preferential reactivation of motivationally relevant information in the ventral striatum. J Neurosci. 2008; 28(25):6372-82. PMC: 3844781. DOI: 10.1523/JNEUROSCI.1054-08.2008. View

Wilson M, McNaughton B . Dynamics of the hippocampal ensemble code for space. Science. 1993; 261(5124):1055-8. DOI: 10.1126/science.8351520. View

10.

Buzsaki G, Leung L, Vanderwolf C . Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 1983; 287(2):139-71. DOI: 10.1016/0165-0173(83)90037-1. View

11.

Zeithamova D, Dominick A, Preston A . Hippocampal and ventral medial prefrontal activation during retrieval-mediated learning supports novel inference. Neuron. 2012; 75(1):168-79. PMC: 3398403. DOI: 10.1016/j.neuron.2012.05.010. View

12.

Benchenane K, Peyrache A, Khamassi M, Tierney P, Gioanni Y, Battaglia F . Coherent theta oscillations and reorganization of spike timing in the hippocampal- prefrontal network upon learning. Neuron. 2010; 66(6):921-36. DOI: 10.1016/j.neuron.2010.05.013. View

13.

Lansink C, Goltstein P, Lankelma J, McNaughton B, Pennartz C . Hippocampus leads ventral striatum in replay of place-reward information. PLoS Biol. 2009; 7(8):e1000173. PMC: 2717326. DOI: 10.1371/journal.pbio.1000173. View

14.

Robbe D, Buzsaki G . Alteration of theta timescale dynamics of hippocampal place cells by a cannabinoid is associated with memory impairment. J Neurosci. 2009; 29(40):12597-605. PMC: 2799373. DOI: 10.1523/JNEUROSCI.2407-09.2009. View

15.

Jackson J, Redish A . Detecting dynamical changes within a simulated neural ensemble using a measure of representational quality. Network. 2003; 14(4):629-45. View

16.

McNaughton B, Battaglia F, Jensen O, Moser E, Moser M . Path integration and the neural basis of the 'cognitive map'. Nat Rev Neurosci. 2006; 7(8):663-78. DOI: 10.1038/nrn1932. View

17.

Hasselmo M, Bower J . Acetylcholine and memory. Trends Neurosci. 1993; 16(6):218-22. DOI: 10.1016/0166-2236(93)90159-j. View

18.

Wikenheiser A, Redish A . The balance of forward and backward hippocampal sequences shifts across behavioral states. Hippocampus. 2012; 23(1):22-9. PMC: 3774294. DOI: 10.1002/hipo.22049. View

19.

Maurer A, McNaughton B . Network and intrinsic cellular mechanisms underlying theta phase precession of hippocampal neurons. Trends Neurosci. 2007; 30(7):325-33. DOI: 10.1016/j.tins.2007.05.002. View

20.

TOLMAN E . Cognitive maps in rats and men. Psychol Rev. 1948; 55(4):189-208. DOI: 10.1037/h0061626. View