Neurodynamics of mental exploration

Contributed by J. J. Hopfield, December 4, 2009 (sent for review October 15, 2009)
December 30, 2009
107 (4) 1648-1653

Abstract

Thinking allows an animal to take an effective action in a novel situation based on a mental exploration of possibilities and previous knowledge. We describe a model animal, with a neural system based loosely on the rodent hippocampus, which performs mental exploration to find a useful route in a spatial world it has previously learned. It then mentally recapitulates the chosen route, and this intent is converted to motor acts that move the animal physically along the route. The modeling is based on spiking neurons with spike-frequency adaptation. Adaptation causes the continuing evolution in the pattern of neural activity that is essential to mental exploration. A successful mental exploration is remembered through spike-timing-dependent synaptic plasticity. The system is also an episodic memory for an animal chiefly concerned with locations.

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Acknowledgments

I thank A.V. Herz, S. Leibler, and C.D. Brody for comments on the manuscript.

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References

1
E Tulving, Episodic memory: From mind to brain. Annu Rev Psychol 53, 1–25 (2000).
2
DO Hebb The Organization of Behavior: A Neuropsychological Theory (Wiley, New York), pp. 153–157 (1949).
3
A Johnson, AD Redish, Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J Neurosci 27, 12176–12189 (2007).
4
EI Moser, E Kropff, M-B Moser, Place cells, grid cells, and the brain's spatial representation system. Annu Rev Neurosci 31, 69–89 (2008).
5
H Eichenbaum, P Dudchenko, E Wood, M Shapiro, H Tanila, The hippocampus, memory, and place cells: Is it spatial memory or a memory space? Neuron 23, 209–226 (1999).
6
V Braitenberg, Cell assemblies in the cerebral cortex. Theoretical Approaches to Complex Systems, Lecture Notes in Biomathematics 21, eds R Heim, G Palm (Springer, Berlin), pp. 171–188 (1978).
7
J O’Keefe, J Dostrovsky, The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34, 171–175 (1971).
8
J O’Keefe, Hippocampal neurophysiology in the behaving animal. The Hippocampus Book, eds P Andersen, R Morris, D Amaral, T Bliss, J O'Keefe (Oxford Univ Press, New York), pp. 487–517 (2007).
9
K Zhang, Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: A theory. J Neurosci 16, 2112–2126 (1996).
10
JJ Hopfield, Neurons with graded response have collective computational properties like those of two-state neurons. Proc Natl Acad Sci USA 81, 3088–3092 (1984).
11
A Samsonovich, BL McNaughton, Path integration and cognitive mapping in a continuous attractor neural network model. J Neurosci 17, 5900–5920 (1997).
12
JJ Hopfield, Searching for memories, Sudoku, implicit check bits, and the iterative use of not-always-correct rapid neural computation. Neural Comput 20, 1119–1164 (2008).
13
N Spruston, C McBain, Structural and functional properties of hippocampal neurons. The Hippocampus Book, eds P Andersen, R Morris, D Amaral, T Bliss, J O'Keefe (Oxford Univ Press, New York), pp. 139–140 (2007).
14
EM Izhikevich, Solving the distal reward problem through linkage of STDP and dopamine signaling. Cereb Cortex 17, 2443–2452 (2007).
15
K Louie, MA Wilson, Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29, 145–156 (2001).
16
K Diba, G Buzsáki, Forward and reverse hippocampal place-cell sequences during ripples. Nat Neurosci 10, 1241–1242 (2007).
17
JE Segall, SM Block, HC Berg, Temporal comparisons in bacterial chemotaxis. Proc Natl Acad Sci USA 83, 8987–8991 (1986).
18
JP Seward, An experimental analysis of latent learning. J Exp Psychol 32, 177–186 (1949).
19
RS Sutton, AG Barto Reinforcement Learning: An Introduction (MIT Press, Cambridge, MA), pp. 5 (1998).

Information & Authors

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Published in

The cover image for PNAS Vol.107; No.4
Proceedings of the National Academy of Sciences
Vol. 107 | No. 4
January 26, 2010
PubMed: 20080534

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Submission history

Published online: December 30, 2009
Published in issue: January 26, 2010

Keywords

  1. hippocampus
  2. memory
  3. planning
  4. thought
  5. hippocampus
  6. memory

Acknowledgments

I thank A.V. Herz, S. Leibler, and C.D. Brody for comments on the manuscript.

Authors

Affiliations

John J. Hopfield
Neuroscience Institute, Carl Icahn Laboratory, Princeton University, Princeton, NJ 08544

Notes

Author contributions: J.J.H. designed research, performed research, analyzed data, and wrote the paper.

Competing Interests

The author declares no conflict of interest.

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    Neurodynamics of mental exploration
    Proceedings of the National Academy of Sciences
    • Vol. 107
    • No. 4
    • pp. 1255-1690

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