Multisensory Control of Hippocampal Spatiotemporal Selectivity

A Sense of Place Hippocampal place cells are believed to be mainly governed by visual and self-motion cues. However, the contribution of sensory cues such as smells, sounds, and textures, etc., is difficult to eliminate. In virtual reality, these cues will not provide any information about the animals' position. Ravassard et al. (p. 1342, published online 2 May) developed a virtual-reality system as immersive and close to the real world as possible and compared place cells in rats running in this apparatus and in the real world. Twice as many neurons were active in a real-world situation compared to virtual reality. While place cells in the real world encoded position, place cells in a virtual world encoded distance. Virtual reality reveals how sensory cues differentially influence brain activity involved in sensing place in rats. The hippocampal cognitive map is thought to be driven by distal visual cues and self-motion cues. However, other sensory cues also influence place cells. Hence, we measured rat hippocampal activity in virtual reality (VR), where only distal visual and nonvestibular self-motion cues provided spatial information, and in the real world (RW). In VR, place cells showed robust spatial selectivity; however, only 20% were track active, compared with 45% in the RW. This indicates that distal visual and nonvestibular self-motion cues are sufficient to provide selectivity, but vestibular and other sensory cues present in RW are necessary to fully activate the place-cell population. In addition, bidirectional cells preferentially encoded distance along the track in VR, while encoding absolute position in RW. Taken together, these results suggest the differential contributions of these sensory cues in shaping the hippocampal population code. Theta frequency was reduced, and its speed dependence was abolished in VR, but phase precession was unaffected, constraining mechanisms governing both hippocampal theta oscillations and temporal coding. These results reveal cooperative and competitive interactions between sensory cues for control over hippocampal spatiotemporal selectivity and theta rhythm.

[1]  B. McNaughton,et al.  The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats , 1983, Experimental Brain Research.

[2]  György Buzsáki,et al.  Hippocampal place cell assemblies are speed-controlled oscillators , 2007, Proceedings of the National Academy of Sciences.

[3]  E. Save,et al.  Contribution of multiple sensory information to place field stability in hippocampal place cells , 2000, Hippocampus.

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

[5]  N. Burgess.  Grid cells and theta as oscillatory interference: Theory and predictions , 2008, Hippocampus.

[6]  H. T. Blair,et al.  Scale-Invariant Memory Representations Emerge from Moiré Interference between Grid Fields That Produce Theta Oscillations: A Computational Model , 2007, The Journal of Neuroscience.

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

[8]  David K Bilkey,et al.  Lesions of the vestibular system disrupt hippocampal theta rhythm in the rat. , 2006, Journal of neurophysiology.

[9]  J. Taube,et al.  Hippocampal spatial representations require vestibular input , 2002, Hippocampus.

[10]  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.

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

[12]  Asohan Amarasingham,et al.  Internally Generated Cell Assembly Sequences in the Rat Hippocampus , 2008, Science.

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

[14]  T. Hafting,et al.  Hippocampus-independent phase precession in entorhinal grid cells , 2008, Nature.

[15]  B. Sakmann,et al.  Phase-locking of hippocampal interneurons' membrane potential to neocortical up-down states , 2006, Nature Neuroscience.

[16]  Sachin S. Deshmukh,et al.  Representation of Non-Spatial and Spatial Information in the Lateral Entorhinal Cortex , 2011, Front. Behav. Neurosci..

[17]  Kamran Diba,et al.  Activity dynamics and behavioral correlates of CA3 and CA1 hippocampal pyramidal neurons , 2012, Hippocampus.

[18]  Lin Tian,et al.  Functional imaging of hippocampal place cells at cellular resolution during virtual navigation , 2010, Nature Neuroscience.

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

[20]  Lisa M. Giocomo,et al.  Grid cell firing may arise from interference of theta frequency membrane potential oscillations in single neurons , 2007, Hippocampus.

[21]  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.

[22]  Giuliano Iurilli,et al.  Sound-Driven Synaptic Inhibition in Primary Visual Cortex , 2012, Neuron.

[23]  Bert Sakmann,et al.  Spontaneous persistent activity in entorhinal cortex modulates cortico-hippocampal interaction in vivo , 2012, Nature Neuroscience.

[24]  B. McNaughton,et al.  Population dynamics and theta rhythm phase precession of hippocampal place cell firing: A spiking neuron model , 1998, Hippocampus.

[25]  M. Diamond,et al.  Sound sensitivity of neurons in rat hippocampus during performance of a sound-guided task. , 2012, Journal of neurophysiology.

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

[27]  K M Gothard,et al.  Dynamics of Mismatch Correction in the Hippocampal Ensemble Code for Space: Interaction between Path Integration and Environmental Cues , 1996, The Journal of Neuroscience.

[28]  Mayank R. Mehta,et al.  The Effects of GluA1 Deletion on the Hippocampal Population Code for Position , 2012, The Journal of Neuroscience.

[29]  M. Quirk,et al.  Experience-Dependent Asymmetric Shape of Hippocampal Receptive Fields , 2000, Neuron.

[30]  B. McNaughton,et al.  Local Sensory Cues and Place Cell Directionality: Additional Evidence of Prospective Coding in the Hippocampus , 2004, The Journal of Neuroscience.