Conjoint control of hippocampal place cell firing by two visual stimuli. I. The effects of moving the stimuli on firing field positions

. 2000 Aug ; 116 (2) : 191-209.

Jazyk angličtina Země Spojené státy americké Médium print

Typ dokumentu časopisecké články, Research Support, U.S. Gov't, P.H.S.

Perzistentní odkaz   https://www.medvik.cz/link/pmid10919866

Grantová podpora
R01 NS020686 NINDS NIH HHS - United States
NS20686 NINDS NIH HHS - United States
NS37150 NINDS NIH HHS - United States

To better understand how hippocampal place cell activity is controlled by sensory stimuli, and to further elucidate the nature of the environmental representation provided by place cells, we have made recordings in the presence of two distinct visual stimuli under standard conditions and after several manipulations of these stimuli. In line with a great deal of earlier work, we find that place cell activity is constant when repeated recordings are made in the standard conditions in which the centers of the two stimuli, a black card and a white card, are separated by 135 degrees on the wall of a cylindrical recording chamber. Rotating the two stimuli by 45 degrees causes equal rotations of place cell firing fields. Removing either card and rotating the other card also causes fields to rotate equally, showing that the two stimuli are individually salient. Increasing or decreasing the card separation (card reconfiguration) causes a topological distortion of the representation of the cylinder floor such that field centers move relative to each other. We also found that either kind of reconfiguration induces a position-independent decrease in the intensity of place cell firing. We argue that these results are not compatible with either of two previously stated views of the place cell representation; namely, a nonspatial theory in which each place cell is tuned to an arbitrarily selected subset of available stimuli or a rigid map theory. We propose that our results imply that the representation is map-like but not rigid; it is capable of undergoing stretches without altering the local arrangement of firing fields.

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Bostock E., Muller R.U., Kubie J.L. Experience-dependent modifications of hippocampal place cell firing. Hippocampus. 1991;1:193–206. PubMed

Burgess N., O'Keefe J. Neuronal computations underlying the firing of place cells and their role in navigation. Hippocampus. 1996;7:749–762. PubMed

Cressant A., Muller R.U., Poucet B. Failure of centrally placed objects to control the firing fields of hippocampal place cells. J. Neurosci. 1997;17:2531–2542. PubMed PMC

Eichenbaum H., Dudchenko P., Wood E., Shapiro M., Tanila H. The hippocampus, memory, and place cellsis it spatial memory or a memory space. Neuron. 1999;23:209–226. PubMed

Fenton A.A., Csizmadia G., Muller R.U. Conjoint control of place cell firing by two visual stimuliII. A vector-field theory. J. Gen. Physiol. 2000;116:211–221. PubMed PMC

Gothard K.M., Skaggs W.E., McNaughton B.L. Dynamics of mismatch correction in the hippocampal ensemble code for spaceinteraction between path integration and environmental cues. J. Neurosci. 1996;16:8027–8040. PubMed PMC

Hetherington P.A., Shapiro M.L. Hippocampal place fields are altered by the removal of single visual cues in a distance-dependent manner. Behav. Neurosci. 1997;111:20–34. PubMed

Kentros C., Hargreaves E., Hawkins R.D., Kandel E.R., Shapiro M., Muller R.U. Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science. 1998;280:2121–2126. PubMed

Knierim J.J., Kudrimoti H.S., McNaughton B.L. Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. J. Neurophysiol. 1998;80:425–446. PubMed

Kubie, J.L., M. Stead, A.A. Fenton, and R.U. Muller. 1996. Methods for improving discrimination of digitally sampled spikes. Soc. Neurosci. Abstr. 22:1870.

Kubie J.L. A drivable bundle of microwires for collecting single-unit data from freely moving rats. Physiol. Behav. 1984;32:115–118. PubMed

Lisman J. Relating hippocampal circuitry to functionrecall of memory sequences by reciprocal dentate-CA3 interactions. Neuron. 1999;22:233–242. PubMed

Markus E.J., Barnes C.A., McNaughton B.L., Gladden V.L., Skaggs W.E. Spatial information content and the reliability of hippocampal CA1 neuronseffects of visual input. Hippocampus. 1994;4:410–421. PubMed

Markus E.J., Qin Y., 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. 1995;15:7079–7094. PubMed PMC

McNaughton B.L., Barnes C.A., Gerrard J.L., Gothard K., Jung M.W., Knierim J.J., Kudrimoti H., Qin Y., Skaggs W.E., Suster M., Weaver K.L. Deciphering the hippocampal polyglotthe hippocampus as a path integration system. J. Exp. Biol. 1996;199:173–185. PubMed

Mizumori S.J.Y., McNaughton B.L., Barnes C.A., Fox K.B. Preserved spatial coding in hippocampal CA1 pyramidal cells during reversible suppression of CA3c outputevidence for pattern completion in hippocampus. J. Neurosci. 1989;9:3915–3928. PubMed PMC

Muller R.U., Bostock E., Taube J., Kubie J.L. On the directional firing properties of hippocampal place cells. J. Neurosci. 1994;14:7235–7251. PubMed PMC

Muller R.U., Kubie J.L. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 1987;7:1951–1968. PubMed PMC

Muller R.U., Kubie J.L. The firing of hippocampal place cells predicts the future position of freely moving rats. J. Neurosci. 1989;9:4101–4110. PubMed PMC

Muller R.U., Kubie J.L., Saypoff R. The hippocampus as a cognitive graph (abridged version) Hippocampus. 1991;1:243–246. PubMed

Muller R.U., Stead M., Pach J. The hippocampus as a cognitive graph. J. Gen. Physiol. 1996;107:663–694. PubMed PMC

O'Keefe J., Burgess N. Geometric determinants of the place fields of hippocampal neurons. Nature. 1996;381:425–428. PubMed

O'Keefe J., Conway D.H. Hippocampal place units in the freely moving ratwhy they fire where they fire. Exp. Brain Res. 1978;31:573–590. PubMed

O'Keefe J., Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971;34:171–175. PubMed

O'Keefe J., Nadel L. The Hippocampus as a Cognitive Map. Clarendon Press; Oxford, UK: 1978.

Paxinos G., Watson M. The rat brain in stereotaxic coordinates. Academic Press, Inc; San Diego, CA: 1986.

Press W.H., Teukolsky S.A., Vetterling W.T., Flannery B.P. Numerical Recipes in C 2nd ed 1992. Cambridge University Press; Cambridge, UK: pp. 623–626

Redish D.A., Touretzky D.S. Cognitive maps beyond the hippocampus. Hippocampus. 1997;7:15–35. PubMed

Rolls E.T. A theory of hippocampal function in memory. Hippocampus. 1996;6:601–620. PubMed

Rotenberg A., Abel T., Hawkins R.D., Kandel E.R., Muller R.U. Parallel instabilities of LTP, place cells and learning caused by decreased protein kinase A activity. J. Neurosci. 2000;In press PubMed PMC

Samsonovich A., McNaughton B.L. Path integration and cognitive mapping in a continuous attractor neural network model. J. Neurosci. 1997;17:5900–5920. PubMed PMC

Save E., Nerad L., Poucet B. Contribution of multiple sensory information to place field stability in hippocampal place cells. Hippocampus. 2000;10:64–76. PubMed

Shapiro M.L., Tanila H., Eichenbaum H. Cues that hippocampal place cells encodedynamic and hierarchical representation of local and distal stimuli. Hippocampus. 1997;7:624–642. PubMed

Sharp P., Muller R.U., Kubie J.L. Firing properties of hippocampal neurons in a visually symmetrical environmentcontributions of multiple sensory cues and mnemonic processes. J. Neurosci. 1990;10:3093–3105. PubMed PMC

Sharp P.E. Computer simulation of hippocampal place cells. Psychobiology. 1991;19:103–115.

Skaggs W.E., McNaughton B.L. Spatial firing properties of hippocampal CA1 populations in an environment containing two visually identical regions. J. Neurosci. 1998;18:8455–8466. PubMed PMC

Skaggs W.E., McNaughton B.L., Gothard K.M., Markus E.J. An information-theoretic approach to deciphering the hippocampal code. In: Hanson S.J., Cowan J.D., Giles C.L., editors. Advances in Neural Information Processing. Vol. 5. Morgan Kaufmann Publishers; San Mateo, CA: 1993. pp. 1030–1037.

Tanila H., Shapiro M., Eichenbaum H. Discordance of spatial representation in ensembles of hippocampal place cells. Hippocampus. 1997;7:613–623. PubMed

Thompson L.T., Best P.J. Place cells and silent cells in the hippocampus of freely-behaving rats. J. Neurosci. 1989;9:2382–2390. PubMed PMC

Thompson L.T., Best P.J. Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Res. 1990;509:299–308. PubMed

Wan H.S., Touretzky D.S., Redish A.D. Towards a computational theory of rat navigation. In: Moser M., Smolensky P., Touretzky D.S., Elman J.L., Weigend A., editors. Proceedings of the 1993 Connectionist Models Summer School. Erlbaum Associates; Hillsdale, NJ: 1993. pp. 11–19.

Zipser D. A computational model of hippocampal place fields. Behav. Neurosci. 1985;99:1006–1018. PubMed

Zinyuk L., Kubik S., Kaminsky Yu., Fenton A.A., Bures J. Understanding hippocampal activity using purposeful behaviorplace navigation induces place cell discharge in both the task-relevant and task-irrelevant spatial reference frames. Proc. Natl. Acad. Sci. USA. 2000;In Press PubMed PMC

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