Abstract
In a recent experimental paper I. Lee et al. [1] showed that the firing patterns of CA1 complex-spike neurons gradually shifted forward across trials toward prospective goal locations within a recording session over multiple trials. Here we propose a simple model of this result based on the phenomenon of awake sequence reverse replay [2] which occurs when the animal pauses at the reward location. The model is based on the CA3-CA1 anatomy with modulation of CA3-CA1 synaptic plasticity by feedback from CA3 projecting CA1 interneurons. Sequence replays, which are generated in CA3 by removal of septal inhibition on CA1 interneurons, are recoded into the synaptic weights of individual CA1 cells. This produces spatially extended CA1 firing fields, whose response provides a value function on experienced paths towards goal locations. Simulations show that the CA1 firing fields show positive movement in center of mass towards reward locations over many trials with negative shift in first few trials, and development of positive skew.
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Lee, I., Griffin, A.L., Zilli, E.A., Eichenbaum, H., Hasselmo, M.E.: Gradual Translocation of Spatial Correlates of Neuronal Firing in the Hippocampus toward Prospective Reward Locations. Neuron 51, 639–650 (2006)
Foster, D.A., Wilson, M.A.: Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440(7084), 615–617 (2006)
Eichenbaum, H.: A cortical-hippocampal system for declarative memory. Nat. Rev. Neurosci. 1, 41–50 (2000)
McClelland, J.L.: Complementary learning systems in the brain. A connectionist approach to explicit and implicit cognition and memory. Ann. N Y Acad. Sci. 843, 153–169 (1998)
O’Keefe, J., Nadel, L.: The hippocampus as a cognitive map. Oxford University Press, Oxford (1978)
Anderson, M.I., Jeffery, K.J.: Heterogeneous modulation of place cell firing by changes in context. J. Neurosci. 23, 8827–8835 (2003)
Gothard, K.M., Skaggs, W.E., Moore, K.M., McNaughton, B.L.: Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J. Neurosci. 16, 823–835 (1996)
Lee, I., Yoganarasimha, D., Rao, G., Knierim, J.J.: Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 430, 456–459 (2004)
Leutgeb, S., Leutgeb, J.K., Treves, A., Moser, M.B., Moser, E.I.: Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305, 1295–1298 (2004)
Breese, C.R., Hampson, R.E., Deadwyler, S.A.: Hippocampal place cells: stereotypy and plasticity. J. Neurosci. 9, 1097–1111 (1989)
Fyhn, M., Molden, S., Hollup, S., Moser, M.B., Moser, E.: Hippocampal neurons responding to first-time dislocation of a target object. Neuron 35, 555–566 (2002)
Kobayashi, T., Nishijo, H., Fukuda, M., Bures, J., Ono, T.: J.Neurophysiol. 78, 597–613 (1997)
Markus, E.J., Qin, Y.L., Leonard, B., Skaggs, W.E., McNaughton, B.L., Barnes, C.A.: Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J.Neurosci. 15, 7079–7094 (1995)
Bower, M.R., Euston, D.R., McNaughton, B.L.: Sequential- context-dependent hippocampal activity is not necessary to learn sequences with repeated elements. J. Neurosci. 25, 1313–1323 (2005)
Ferbinteanu, J., Shapiro, M.L.: Prospective and retrospective memory coding in the hippocampus. Neuron 40(2003), 1227–1239 (2003)
Wood, E.R., Dudchenko, P.A., Robitsek, R.J., Eichenbaum, H.: Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27, 623–633 (2000)
Freund, T., Buzsaki, G.: Interneurons of the Hippocampus. Hippocampus 6, 347–470 (1996)
Sik, A., Minen, A., Penttonen, M., Buzsaki, G.: Inhibitory CA1-CA3- hilar region feedback in the hippocampus. Science 265, 1722–1724 (1994)
Somoyogi, P., Klausberger, T.: Defined types of cortical interneurone structure space and time in the Hippocampus. J.Physiol. 562.1, 9–26 (2005)
Foster, D.J., Wilson, M.A.: Hippocampal theta sequences Hippocampus (2007), DOI 10.1002/hipo.20345
Lisman, J.E.: Relating Hippocampal Circuitry to Function: Recall of Memory Sequences by Reciprocal Dentate-CA3 Interactions. Neuron 22, 233–242 (1999)
Johnston, D., Amaral, D.G.: In: Shepard, G.M. (ed.) The Synaptic Organization of the Brain, Oxford University Press, Oxford (1998)
Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., Moser, E.I.: Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801 (2005)
Freund, T., Antal, M.: GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336, 170–173 (1998)
Ponzi, A.: Dynamical System Model of Spatial Reward Learning. IEICE Technical Report 103, 163, 19–24 (2006)
Ponzi, A.: Model of Balance of Excitation and Inhibition in Hippocampal Sharp Wave Replays and Application to Spatial Remapping. In: Proceedings of IJCNN 2007 (2007)
Ponzi, A.: Simple Model of Hippocampal Splitter Cells. Japan Neural Network Society (JNNS) abstract (2006)
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Ponzi, A. (2008). Neural Network Model of Forward Shift of CA1 Place Fields Towards Reward Location. In: Ishikawa, M., Doya, K., Miyamoto, H., Yamakawa, T. (eds) Neural Information Processing. ICONIP 2007. Lecture Notes in Computer Science, vol 4984. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-69158-7_33
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DOI: https://doi.org/10.1007/978-3-540-69158-7_33
Publisher Name: Springer, Berlin, Heidelberg
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