Changing the angular separation between two visual stimuli attached to the wall of a recording cylinder causes the firing fields of place cells to move relative to each other, as though the representation of the floor undergoes a topological distortion. The displacement of the firing field center of each cell is a vector whose length is equal to the linear displacement and whose angle indicates the direction that the field center moves in the environment. Based on the observation that neighboring fields move in similar ways, whereas widely separated fields tend to move relative to each other, we develop an empirical vector-field model that accounts for the stated effects of changing the card separation. We then go on to show that the same vector-field equation predicts additional aspects of the experimental results. In one example, we demonstrate that place cell firing fields undergo distortions of shape after the card separation is changed, as though different parts of the same field are affected by the stimulus constellation in the same fashion as fields at different locations. We conclude that the vector-field formalism reflects the organization of the place-cell representation of the environment for the current case, and through suitable modification may be very useful for describing motions of firing patterns induced by a wide variety of stimulus manipulations.

Institute of Physiology Academy of Sciences of the Czech Republic Prague

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Andersen P., Eccles J.C., Loyning Y. Pathway of postsynaptic inhibition in the hippocampus. J. Neurophysiol. 1964;27:608–619. PubMed

Blum K.I., Abbott L.F. A model of spatial map formation in the hippocampus of the rat. Neural Computat. 1996;8:85–93. PubMed

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

Brown J.E., Skaggs W.E. Discordant coding of spatial location in the rat hippocampus. Soc. Neurosci. Abstr. 1999;556:1381.

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

Eichenbaum H. Is the rodent hippocampus just for “place”? Curr. Opin. Neurobiol. 1996;6:187–195. PubMed

Fenton A.A., Muller R.U. Place cell discharge is extremely variable during individual passes of the rat through the firing field. Proc. Natl. Acad. Sci. USA. 1998;95:3182–3187. PubMed PMC

Fenton A.A., Csizmadia G., Muller R.U. Conjoint control of hippocampal place cell firing by two visual stimuliI. The effects of moving the stimuli on firing field positions. J. Gen. Physiol. 2000;116:191–209. PubMed PMC

Fox S.E., Ranck J.B., Jr. Localization and anatomical identification of theta and complex spike cells in the dorsal hippocampal formation of rats. Exp. Neurol. 1975;49:299–313. PubMed

Freund T.F., Buzsaki G. Interneurons of the hippocampus. Hippocampus. 1996;6:347–470. PubMed

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

Kubie J.L., Muller R.U., Bostock E. Spatial firing properties of hippocampal theta cells. J. Neurosci. 1990;10:1110–1123. PubMed PMC

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

Mehta M.R., Barnes C.A., McNaughton B.L. Experience-dependent, asymmetric expansion of hippocampal place fields. Proc. Natl. Acad. Sci. USA. 1997;9:8918–8921. 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. A quarter century of place cells. Neuron. 1996;17:813–822. PubMed

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., Csizmadia G., Fenton A.A. A vector field model that accounts for movements of place cell firing fields accurately changes of field shapes. Soc. Neurosci. Abstr. 1998;559:1417.

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. Do hippocampal pyramidal cells signal non-spatial as well as spatial information? Hippocampus. 1999;9:352–364. PubMed

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

Ranck J.B., Jr. Studies on single neurons in dorsal hippocampal formation and septum of unrestrained rats. Part I. Behavioral correlates and firing repertoires. Exp. Neurol. 1973;41:461–555. PubMed

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

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. Complimentary roles for hippocampal versus subicular/entorhinal place cells in coding place, context and events. Hippocampus. 1999;9:432–443. PubMed

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

Taube J.S., Muller R.U., Ranck J.B., Jr. Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J. Neurosci. 1990;10:436–447. PubMed PMC

Taube J. Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J. Neurosci. 1994;15:70–86. PubMed PMC

Wood E.R., Dudchenko P.A., Eichenbaum H. The global record of memory in hippocampal neuronal activity. Nature. 1999;397:613–616. PubMed

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