Spatial representations of self and other in the hippocampus

The representation of others in space Different sets of neurons encode the spatial position and orientation of an organism. However, social animals need to know the position of other individuals for social interactions, observational learning, and group navigation. Surprisingly, very little is known about how the position of other animals is represented in the brain. Danjo et al. and Omer et al. now report the discovery of a subgroup of neurons in hippocampal area CA1 that encodes the presence of conspecifics in rat and bat brains, respectively. Science, this issue p. 213, p. 218 A group of neurons in hippocampal area CA1 of rats represents the position of conspecifics. An animal’s awareness of its location in space depends on the activity of place cells in the hippocampus. How the brain encodes the spatial position of others has not yet been identified. We investigated neuronal representations of other animals’ locations in the dorsal CA1 region of the hippocampus with an observational T-maze task in which one rat was required to observe another rat’s trajectory to successfully retrieve a reward. Information reflecting the spatial location of both the self and the other was jointly and discretely encoded by CA1 pyramidal cells in the observer rat. A subset of CA1 pyramidal cells exhibited spatial receptive fields that were identical for the self and the other. These findings demonstrate that hippocampal spatial representations include dimensions for both self and nonself.

[1]  E. Tolman Cognitive maps in rats and men. , 1948, Psychological review.

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

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

[4]  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.

[5]  J. O’Keefe,et al.  Phase relationship between hippocampal place units and the EEG theta rhythm , 1993, Hippocampus.

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

[7]  G. Rizzolatti,et al.  Action recognition in the premotor cortex. , 1996, Brain : a journal of neurology.

[8]  B L McNaughton,et al.  Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. , 1998, Journal of neurophysiology.

[9]  E N Brown,et al.  A Statistical Paradigm for Neural Spike Train Decoding Applied to Position Prediction from Ensemble Firing Patterns of Rat Hippocampal Place Cells , 1998, The Journal of Neuroscience.

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

[11]  H. Eichenbaum,et al.  The global record of memory in hippocampal neuronal activity , 1999, Nature.

[12]  M. Wilson,et al.  Trajectory Encoding in the Hippocampus and Entorhinal Cortex , 2000, Neuron.

[13]  H. Eichenbaum,et al.  Hippocampal Neurons Encode Information about Different Types of Memory Episodes Occurring in the Same Location , 2000, Neuron.

[14]  E. Maguire,et al.  The Human Hippocampus and Spatial and Episodic Memory , 2002, Neuron.

[15]  M. R. Mehta,et al.  Role of experience and oscillations in transforming a rate code into a temporal code , 2002, Nature.

[16]  L. Frank,et al.  Single Neurons in the Monkey Hippocampus and Learning of New Associations , 2003, Science.

[17]  Arne D. Ekstrom,et al.  Cellular networks underlying human spatial navigation , 2003, Nature.

[18]  J. Knierim,et al.  Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3 , 2004, Nature.

[19]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[20]  Neil Burgess,et al.  Attractor Dynamics in the Hippocampal Representation of the Local Environment , 2005, Science.

[21]  B. McNaughton,et al.  Independent Codes for Spatial and Episodic Memory in Hippocampal Neuronal Ensembles , 2005, Science.

[22]  C. Koch,et al.  Invariant visual representation by single neurons in the human brain , 2005, Nature.

[23]  T. Hafting,et al.  Microstructure of a spatial map in the entorhinal cortex , 2005, Nature.

[24]  G. Buzsáki,et al.  Temporal Encoding of Place Sequences by Hippocampal Cell Assemblies , 2006, Neuron.

[25]  David J. Foster,et al.  Reverse replay of behavioural sequences in hippocampal place cells during the awake state , 2006, Nature.

[26]  Bruce L. McNaughton,et al.  Path integration and the neural basis of the 'cognitive map' , 2006, Nature Reviews Neuroscience.

[27]  G. Buzsáki,et al.  Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex , 2008, Nature Neuroscience.

[28]  S. A. Ho,et al.  Hippocampal place cell activity during chasing of a moving object associated with reward in rats , 2008, Neuroscience.

[29]  Philipp Berens,et al.  CircStat: AMATLABToolbox for Circular Statistics , 2009, Journal of Statistical Software.

[30]  D. Tank,et al.  Intracellular dynamics of hippocampal place cells during virtual navigation , 2009, Nature.

[31]  Asohan Amarasingham,et al.  Conditional modeling and the jitter method of spike resampling. , 2012, Journal of neurophysiology.

[32]  Sachin S. Deshmukh,et al.  Influence of local objects on hippocampal representations: Landmark vectors and memory , 2013, Hippocampus.

[33]  Mayank R. Mehta,et al.  Multisensory Control of Hippocampal Spatiotemporal Selectivity , 2013, Science.

[34]  G. Buzsáki,et al.  Memory, navigation and theta rhythm in the hippocampal-entorhinal system , 2013, Nature Neuroscience.

[35]  Eran Stark,et al.  Large-scale, high-density (up to 512 channels) recording of local circuits in behaving animals. , 2014, Journal of neurophysiology.

[36]  S. Siegelbaum,et al.  The hippocampal CA2 region is essential for social memory , 2014, Nature.

[37]  Kenneth D. Harris,et al.  High-Dimensional Cluster Analysis with the Masked EM Algorithm , 2013, Neural Computation.

[38]  Edvard I. Moser,et al.  Speed cells in the medial entorhinal cortex , 2015, Nature.

[39]  Dheeraj S. Roy,et al.  Ventral CA1 neurons store social memory , 2016, Science.

[40]  Daoyun Ji,et al.  Social observation enhances cross-environment activation of hippocampal place cell patterns , 2016, eLife.

[41]  H. Eichenbaum,et al.  Medial Entorhinal Cortex Selectively Supports Temporal Coding by Hippocampal Neurons , 2017, Neuron.