Entorhinal Place Cells: Trajectory Encoding

  • Loren M. Frank
  • Emery N. Brown
  • Matthew A. Wilson

Abstract

If an animal is to successfully navigate through its environment it must not only know where it is, but also where it has been, where it should go, and the relationship among positions in its environment. An animal scavenging for food, for example, needs to remember the set of locations it has visited so that it does waste time retracing its steps. In addition, unless food is randomly scattered through the environment, the animal must be able to learn and remember the locations that are most likely to contain food. Furthermore, the animal must know the relationship between its current position and those locations so that it can plan and execute the movements necessary for it to reach its goals. Our task, then, is to relate neural activity in the brain to the specific requirements of goal directed navigation: knowledge of current, past, and future position, and knowledge of the relationships among positions. Here we will examine how a rat’s movements through its environment relate to neural activity in the CA1 region of the hippocampus and in the entorhinal cortex, the primary source of neocortically derived input to the hippocampus and the primary target of neocortically bound hippocampal outputs.

Keywords

Hunt Arena 

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References

  1. Aggleton JP, Hunt PR, Rawlins JN (1986) The effects of hippocampal lesions upon spatial and non-spatial tests of working memory. Behav Brain Res 19: 133–146.PubMedCrossRefGoogle Scholar
  2. Amaral DG, Witter MP (1995) Hippocampal Formation. In: The Rat Nervous System (Paxinos C, ed), pp 443–493. Academic Press.Google Scholar
  3. Barnes CA, McNaughton BL, Mizumori SJ, Leonard BW, Lin LH (1990) Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. Prog Brain Res 83:287–300: 287–300.PubMedCrossRefGoogle Scholar
  4. Brown EN, Frank LM, Tang D, Quirk MC, Wilson MA (1998) A statistical paradigm for neural spike train decoding applied to position prediction from ensemble firing patterns of rat hippocampal place cells. J Neurosci 18: 7411–7425.PubMedGoogle Scholar
  5. Brumberg JC, Pinto DJ, Simons DJ (1996) Spatial gradients and inhibitory summation in the rat whisker barrel system. J Neurophysiol 76: 130–140.PubMedGoogle Scholar
  6. Eichenbaum H (2000) Hippocampus: mapping or memory? Curr Biol 10: R785–R787.PubMedCrossRefGoogle Scholar
  7. Fox SE, Ranck JBJ (1981) Electrophysiological characteristics of hippocampal complex-spike cells and theta cells. Exp Brain Res 41: 399–410.PubMedCrossRefGoogle Scholar
  8. Frank LM, Brown EN, Wilson MA (2000) Trajectory Encoding in the Hippocampus and Entorhinal Cortex. Neuron 27: 169–178.PubMedCrossRefGoogle Scholar
  9. Gray CM, Maldonado PE, Wilson M, McNaughton B (1995) Tetrodes markedly improve the reliability and yield of multiple single- unit isolation from multi-unit recordings in cat striate cortex. J Neurosci Methods 63: 43–54.PubMedCrossRefGoogle Scholar
  10. Insausti R, Herrero MT, Witter MP (1997) Entorhinal cortex of the rat: cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus 7: 146–183.PubMedCrossRefGoogle Scholar
  11. Markus EJ, Qin YL, Leonard B, Skaggs WE, McNaughton BL, Barnes CA (1995) Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J Neurosci 15: 7079–7094.PubMedGoogle Scholar
  12. McCormick DA, Connors BW, Lighthall JW, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54: 782–806.PubMedGoogle Scholar
  13. McNaughton BL, Barnes CA, O’Keefe J (1983) The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res 52: 41–49.PubMedCrossRefGoogle Scholar
  14. Mizumori SJ, Ward KE, Lavoie AM (1992) Medial septal modulation of entorhinal single unit activity in anesthetized and freely moving rats. Brain Res 570: 188–197.PubMedCrossRefGoogle Scholar
  15. Morris RG, Anderson E, Lynch GS, Baudry M (1986) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319: 774–776.PubMedCrossRefGoogle Scholar
  16. Quirk G J, Muller RU, Kubie JL, Ranck JB, Jr. (1992) The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells. J Neurosci 12: 1945–1963.PubMedGoogle Scholar
  17. Rao SG, Williams GV, Goldman-Rakic PS (1999) Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. J Neurophysiol 81: 1903–1916.PubMedGoogle Scholar
  18. Rawlins JN, Olton DS (1982) The septo-hippocampal system and cognitive mapping. Behav Brain Res 5: 331–358.PubMedCrossRefGoogle Scholar
  19. Sharp PE (1997) Subicular cells generate similar spatial firing patterns in two geometrically and visually distinctive environments: comparison with hippocampal place cells. Behav Brain Res 85: 71–92.PubMedCrossRefGoogle Scholar
  20. Sharp PE (1999) Subicular place cells expand or contract their spatial firing pattern to fit the size of the environment in an open field but not in the presence of barriers: comparison with hippocampal place cells. Behav Neurosci 113: 643–662.PubMedCrossRefGoogle Scholar
  21. Sharp PE, Green C (1994) Spatial correlates of firing patterns of single cells in the subiculum of the freely moving rat. J Neurosci 14: 2339–2356.PubMedGoogle Scholar
  22. Simons DJ (1978) Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophysiol 41: 798–820.PubMedGoogle Scholar
  23. Skaggs WE, McNaughton BL, Gothard K, Markus EJ (1993) An information-theoretic approach to deciphering the hippocampal code. In: Advances in neural information processing 5 (Hanson SJ, Cowan JD, Giles CL, eds), pp 1030–1037. San Mateo, CA: Morgan Kaufman.Google Scholar
  24. Swadlow HA, Beloozerova IN, Sirota MG (1998) Sharp, local synchrony among putative feed-forward inhibitory interneurons of rabbit somatosensory cortex. J Neurophysiol 79: 567–582.PubMedGoogle Scholar
  25. Taube JS, Muller RU, Ranck JBJ (1990) Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci 10: 420–435.PubMedGoogle Scholar
  26. Wilson FA, O’Scalaidhe SP, Goldman-Rakic PS (1994) Functional synergism between putative gamma-aminobutyrate-containing neurons and pyramidal neurons in prefrontal cortex. Proc Natl Acad Sci U S A 91: 4009–4013.PubMedCrossRefGoogle Scholar
  27. Witter MP, Groenewegen HJ, da FH, Lohman AH (1989) Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol 33: 161–253.PubMedCrossRefGoogle Scholar
  28. Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H (2000) Hippocampal neurons encode information about different types of memory episodes occurring in the same location [In Process Citation]. Neuron 27: 623–633.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • Loren M. Frank
    • 1
  • Emery N. Brown
    • 1
  • Matthew A. Wilson
    • 2
  1. 1.Massachusetts General HospitalUSA
  2. 2.Massachusetts Institute of TechnologyUSA

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