Dynamics of Mismatch Correction in the Hippocampal Ensemble Code for Space: Interaction between Path Integration and Environmental Cues

Populations of hippocampal neurons were recorded simultaneously in rats shuttling on a track between a fixed reward site at one end and a movable reward site, mounted in a sliding box, at the opposite end. While the rat ran toward the fixed site, the box was moved. The rat returned to the box in its new position. On the initial part of all journeys, cells fired at fixed distances from the origin, whereas on the final part, cells fired at fixed distances from the destination. Thus, on outward journeys from the box, with the box behind the rat, the position representation must have been updated by path integration. Farther along the journey, the place field map became aligned on the basis of external stimuli. The spatial representation was quantified in terms of population vectors. During shortened journeys, the vector shifted from an alignment with the origin to an alignment with the destination. The dynamics depended on the degree of mismatch with respect to the full-length journey. For small mismatches, the vector moved smoothly through intervening coordinates until the mismatch was corrected. For large mismatches, it jumped abruptly to the new coordinate. Thus, when mismatches occur, path integration and external cues interact competitively to control place-cell firing. When the same box was used in a different environment, it controlled the alignment of a different set of place cells. These data suggest that although map alignment can be controlled by landmarks, hippocampal neurons do not explicitly represent objects or events.

[1]  D. Touretzky,et al.  Cognitive maps beyond the hippocampus , 1997, Hippocampus.

[2]  J. B. Ranck,et al.  Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. , 1973, Experimental neurology.

[3]  Roland Maurer,et al.  What is modelling for? a critical review of the models of path integration , 1995 .

[4]  R. Muller,et al.  Firing properties of hippocampal neurons in a visually symmetrical environment: contributions of multiple sensory cues and mnemonic processes , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  R Worden,et al.  Navigation by fragment fitting: A theory of hippocampal function , 1992, Hippocampus.

[6]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[7]  B. McNaughton,et al.  Place cells, head direction cells, and the learning of landmark stability , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  J. O’Keefe,et al.  Geometric determinants of the place fields of hippocampal neurons , 1996, Nature.

[9]  W. Chambers,et al.  Reflexes involving triceps surae from the ankle joint of the cat. , 1973, Experimental neurology.

[10]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

[11]  H. Eichenbaum,et al.  Correlates of hippocampal complex-spike cell activity in rats performing a nonspatial radial maze task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  H Eichenbaum,et al.  The organization of spatial coding in the hippocampus: a study of neural ensemble activity , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  H. Eichenbaum,et al.  Representation in the hippocampus: what do hippocampal neurons code? , 1988, Trends in Neurosciences.

[14]  Terrence J. Sejnowski,et al.  ASSOCIATIVE MEMORY AND HIPPOCAMPAL PLACE CELLS , 1995 .

[15]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[16]  C. Barnes Spatial learning and memory processes: the search for their neurobiological mechanisms in the rat , 1988, Trends in Neurosciences.

[17]  H. Eichenbaum,et al.  Neuronal activity in the hippocampus during delayed non‐match to sample performance in rats: Evidence for hippocampal processing in recognition memory , 1992, Hippocampus.

[18]  R. Hampson,et al.  Hippocampal cell firing correlates of delayed-match-to-sample performance in the rat. , 1993, Behavioral neuroscience.

[19]  B. McNaughton,et al.  Spatial information content and reliability of hippocampal CA1 neurons: Effects of visual input , 1994, Hippocampus.

[20]  D. Olton,et al.  Spatial correlates of hippocampal unit activity , 1978, Experimental Neurology.

[21]  M. Kuperstein,et al.  Cue-sampling and goal-approach correlates of hippocampal unit activity in rats performing an odor-discrimination task , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  W E Skaggs,et al.  Interactions between location and task affect the spatial and directional firing of hippocampal neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  R. Muller,et al.  On the directional firing properties of hippocampal place cells , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  R. Muller,et al.  The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  R. Hampson,et al.  Hippocampal place cells: stereotypy and plasticity , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[27]  R U Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  L. Jarrard On the role of the hippocampus in learning and memory in the rat. , 1993, Behavioral and neural biology.

[29]  H. Eichenbaum,et al.  Spatial and behavioral correlates of hippocampal neuronal activity , 1989 .

[30]  W E Skaggs,et al.  Deciphering the hippocampal polyglot: the hippocampus as a path integration system. , 1996, The Journal of experimental biology.

[31]  Roland Maurer,et al.  Short-distance homing in the golden hamster after a passive outward journey , 1986, Animal Behaviour.

[32]  B. McNaughton,et al.  Spatial selectivity of unit activity in the hippocampal granular layer , 1993, Hippocampus.

[33]  B L McNaughton,et al.  Dynamics of the hippocampal ensemble code for space. , 1993, Science.

[34]  R. Muller,et al.  The firing of hippocampal place cells in the dark depends on the rat's recent experience , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  A. Etienne Navigation of a Small Mammal by Dead Reckoning and Local Cues , 1992 .

[36]  J. O’Keefe Place units in the hippocampus of the freely moving rat , 1976, Experimental Neurology.

[37]  J. Taube Head direction cells recorded in the anterior thalamic nuclei of freely moving rats , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  Horst Mittelstaedt,et al.  Homing by Path Integration , 1982 .

[39]  R. Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  J. B. Ranck,et al.  Spatial firing patterns of hippocampal complex-spike cells in a fixed environment , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  K M Gothard,et al.  Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  K. Cheng A purely geometric module in the rat's spatial representation , 1986, Cognition.

[43]  R. Muller,et al.  The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.