Convergence of Head Direction and Place Information in the Ca1 Region of Hippocampus Subjects and Behavioral Testing

The hippocampus has long been considered critical for spatial learning and navigation. Recent theoretical models of the rodent and primate hippocampus consider spatial processing a special case of a more general memory function. These non-spatial theories of hippocampus differ from navigational theories with respect to the role of self-motion representations. The present study presents evidence for a new cell type in the CA1 area of the rat hippocampus that codes for directional heading independent of location information (i.e. the angular component of self-motion). These hippocampal head direction cells are controlled by external and idiothetic cues in a similar way as head direction cells in other brain areas and hippocampal place cells. Convergent head direction information and location information may be an essential component of a neural system that monitors behavioral sequences during navigation. Conflicts between internally generated and external cues have previously been shown to result in new hippocampal place representations, suggesting that head direction information may participate in synaptic interactions when new location codes are formed. Combined hippocampal representations of self-motion and external cues may therefore contribute to path integration as well as spatial memory processing.

[1]  U. Frey,et al.  Hippocampal synaptic plasticity: role in spatial learning or the automatic recording of attended experience? , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[3]  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.

[4]  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.

[5]  J. Csicsvari,et al.  Oscillatory Coupling of Hippocampal Pyramidal Cells and Interneurons in the Behaving Rat , 1999, The Journal of Neuroscience.

[6]  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.

[7]  G. Buzsáki,et al.  Inhibitory CA1-CA3-hilar region feedback in the hippocampus. , 1994, Science.

[8]  R. Plonsey,et al.  The extracellular potential field of the single active nerve fiber in a volume conductor. , 1968, Biophysical journal.

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

[10]  P E Sharp,et al.  Influences of vestibular and visual motion information on the spatial firing patterns of hippocampal place cells , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  B. McNaughton,et al.  Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. , 1998, Journal of neurophysiology.

[12]  S. Mizumori,et al.  Medial septal modulation of entorhinal single unit activity in anesthetized and freely moving rats , 1992, Brain Research.

[13]  J. Struijk,et al.  The extracellular potential of a myelinated nerve fiber in an unbounded medium and in nerve cuff models. , 1997, Biophysical journal.

[14]  C. Köhler Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex , 1985, The Journal of comparative neurology.

[15]  Michael Recce,et al.  A model of hippocampal function , 1994, Neural Networks.

[16]  Chris J. McBain,et al.  Glutamatergic synapses onto hippocampal interneurons: precision timing without lasting plasticity , 1999, Trends in Neurosciences.

[17]  J. Taube,et al.  Head direction cells and episodic spatial information in rats without a hippocampus. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[18]  E. Rolls,et al.  Head direction cells in the primate pre‐subiculum , 1999, Hippocampus.

[19]  S. Mizumori,et al.  Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  J. B. Ranck,et al.  Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. II. Hippocampal slow waves and theta cell firing during bar pressing and other behaviors. , 1973, Experimental neurology.

[21]  Jeffrey S. Taube,et al.  Preferential use of the landmark navigational system by head direction cells in rats. , 1995 .

[22]  B. McNaughton,et al.  Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. , 1990, Progress in brain research.

[23]  J. Taube,et al.  Correlation between head direction cell activity and spatial behavior on a radial arm maze. , 1997 .

[24]  J S Taube,et al.  Correlation between head direction cell activity and spatial behavior on a radial arm maze. , 1997, Behavioral neuroscience.

[25]  T. van Groen,et al.  The connections of presubiculum and parasubiculum in the rat , 1990, Brain Research.

[26]  J. Taube,et al.  Interaction between the Postsubiculum and Anterior Thalamus in the Generation of Head Direction Cell Activity , 1997, The Journal of Neuroscience.

[27]  S. Wise,et al.  Role of the Hippocampal System in Conditional Motor Learning: Mapping Antecedents to Action , 1999, Hippocampus.

[28]  S J Mizumori,et al.  Redistribution of spatial representation in the hippocampus of aged rats performing a spatial memory task. , 1996, Behavioral neuroscience.

[29]  G. H. Bishop,et al.  THE SIZE OF NERVE FIBERS SUPPLYING CEREBRAL CORTEX. , 1964, Experimental neurology.

[30]  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.

[31]  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.

[32]  H. T. Blair,et al.  Anticipatory head direction signals in anterior thalamus: evidence for a thalamocortical circuit that integrates angular head motion to compute head direction , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  G Buzsáki,et al.  Sustained activation of hippocampal pyramidal cells by ‘space clamping’ in a running wheel , 1999, The European journal of neuroscience.

[34]  David Gaffan,et al.  Idiothetic input into object-place configuration as the contribution to memory of the monkey and human hippocampus: a review , 1998, Experimental Brain Research.

[35]  W. Cowan,et al.  An autoradiographic study of the organization of the efferet connections of the hippocampal formation in the rat , 1977, The Journal of comparative neurology.

[36]  A. Berthoz,et al.  Neurons responding to whole-body motion in the primate hippocampus , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  Kathryn J Jeffery,et al.  Learning of landmark stability and instability by hippocampal place cells , 1998, Neuropharmacology.

[38]  S. Mizumori,et al.  Excitotoxic Septal Lesions Result in Spatial Memory Deficits and Altered Flexibility of Hippocampal Single-Unit Representations , 1999, The Journal of Neuroscience.

[39]  C. H. Vanderwolf,et al.  Hippocampal electrical activity and voluntary movement in the rat. , 1969, Electroencephalography and clinical neurophysiology.

[40]  I. Whishaw,et al.  Evidence for extrahippocampal involvement in place learning and hippocampal involvement in path integration , 1996, Hippocampus.

[41]  D. Humphrey,et al.  Extracellular Single-Unit Recording Methods , 1990 .

[42]  J. Michael Wyass,et al.  Connections between the retrosplenial cortex and the hippocampal formation in the rat: A review , 1992, Hippocampus.

[43]  J S Taube,et al.  Head Direction Cells in Rats with Hippocampal or Overlying Neocortical Lesions: Evidence for Impaired Angular Path Integration , 1999, The Journal of Neuroscience.

[44]  J S Taube,et al.  Preferential use of the landmark navigational system by head direction cells in rats. , 1995, Behavioral neuroscience.

[45]  J. Clark,et al.  Extracellular currents and potentials of the active myelinated nerve fiber. , 1987, Biophysical journal.

[46]  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.

[47]  H. Eichenbaum,et al.  The Hippocampus, Memory, and Place Cells Is It Spatial Memory or a Memory Space? , 1999, Neuron.

[48]  G. Buzsáki,et al.  Interneurons of the hippocampus , 1998, Hippocampus.