Linear Self-Motion Cues Support the Spatial Distribution and Stability of Hippocampal Place Cells

The vestibular system provides a crucial component of place-cell and head-direction cell activity [1-7]. Otolith signals are necessary for head-direction signal stability and associated behavior [8, 9], and the head-direction signal's contribution to parahippocampal spatial representations [10-14] suggests that place cells may also require otolithic information. Here, we demonstrate that self-movement information from the otolith organs is necessary for the development of stable place fields within and across sessions. Place cells in otoconia-deficient tilted mice showed reduced spatial coherence and formed place fields that were located closer to environmental boundaries, relative to those of control mice. These differences reveal an important otolithic contribution to place-cell functioning and provide insight into the cognitive deficits associated with otolith dysfunction.

[1]  Noah A. Russell,et al.  Long-Term Effects of Permanent Vestibular Lesions on Hippocampal Spatial Firing , 2003, The Journal of Neuroscience.

[2]  Douglas G Wallace,et al.  Otolithic information is required for homing in the mouse , 2015, Hippocampus.

[3]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

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

[5]  James J Knierim,et al.  Dominance of the proximal coordinate frame in determining the locations of hippocampal place cell activity during navigation. , 2008, Journal of neurophysiology.

[6]  Denise Manahan-Vaughan,et al.  Spatial Olfactory Learning Contributes to Place Field Formation in the Hippocampus , 2013, Cerebral cortex.

[7]  J. Taube,et al.  Head Direction Cell Activity in Mice: Robust Directional Signal Depends on Intact Otolith Organs , 2009, The Journal of Neuroscience.

[8]  B. J. Clark,et al.  Disruption of the head direction cell network impairs the parahippocampal grid cell signal , 2015, Science.

[9]  Seth L. Kirby,et al.  Otoconia‐deficient mice show selective spatial deficits , 2014, Hippocampus.

[10]  Charlotte N. Boccara,et al.  Grid cells in pre- and parasubiculum , 2010, Nature Neuroscience.

[11]  Ryan E. Harvey,et al.  Post-training Inactivation of the Anterior Thalamic Nuclei Impairs Spatial Performance on the Radial Arm Maze , 2017, Front. Neurosci..

[12]  Douglas G Wallace,et al.  Vestibular Information Is Required for Dead Reckoning in the Rat , 2002, The Journal of Neuroscience.

[13]  B. McNaughton,et al.  Self-Motion and the Hippocampal Spatial Metric , 2005, The Journal of Neuroscience.

[14]  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.

[15]  Robert U Muller,et al.  Head direction cells: properties and functional significance , 1996, Current Opinion in Neurobiology.

[16]  J. B. Ranck,et al.  Electrophysiological characteristics of hippocampal complex-spike cells and theta cells , 2004, Experimental Brain Research.

[17]  Edvard I Moser,et al.  Development of the Spatial Representation System in the Rat , 2010, Science.

[18]  Thomas J. Wills,et al.  Development of the Hippocampal Cognitive Map in Preweanling Rats , 2010, Science.

[19]  B. McNaughton,et al.  Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex , 1995, Journal of Neuroscience Methods.

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

[21]  Benjamin J. Clark,et al.  Do the anterior and lateral thalamic nuclei make distinct contributions to spatial representation and memory? , 2016, Neurobiology of Learning and Memory.

[22]  J. Taube,et al.  Behavioral/systems/cognitive Hippocampal Place Cell Instability after Lesions of the Head Direction Cell Network , 2022 .

[23]  M. Yartsev,et al.  Grid cells without theta oscillations in the entorhinal cortex of bats , 2011, Nature.

[24]  Sarah Bate,et al.  The Cognitive Neuroscience of Face Processing , 2013 .

[25]  Ryan M. Yoder,et al.  Otolith dysfunction alters exploratory movement in mice , 2017, Behavioural Brain Research.

[26]  G. W. Harding,et al.  Otoconial agenesis in tilted mutant mice , 1998, Hearing Research.

[27]  Bruce L. McNaughton,et al.  An Information-Theoretic Approach to Deciphering the Hippocampal Code , 1992, NIPS.

[28]  M. Moser,et al.  Representation of Geometric Borders in the Entorhinal Cortex , 2008, Science.

[29]  L M Frank,et al.  A comparison of the firing properties of putative excitatory and inhibitory neurons from CA1 and the entorhinal cortex. , 2001, Journal of neurophysiology.

[30]  Bruce L. McNaughton,et al.  The stereotrode: A new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records , 1983, Journal of Neuroscience Methods.

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

[32]  Sachin S. Deshmukh,et al.  Theta modulation in the medial and the lateral entorhinal cortices. , 2010, Journal of neurophysiology.

[33]  J. Baker,et al.  The vestibulo ocular reflex (VOR) in otoconia deficient head tilt (het) mutant mice versus wild type C57BL/6 mice , 2003, Brain Research.

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

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

[36]  Roddy M. Grieves,et al.  Lesions of the Head Direction Cell System Increase Hippocampal Place Field Repetition , 2017, Current Biology.

[37]  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.

[38]  G. Buzsáki.  Theta Oscillations in the Hippocampus , 2002, Neuron.

[39]  J. Knierim,et al.  Major Dissociation Between Medial and Lateral Entorhinal Input to Dorsal Hippocampus , 2005, Science.

[40]  J. Knierim,et al.  Coupling between place cells and head direction cells during relative translations and rotations of distal landmarks , 2004, Experimental Brain Research.

[41]  Jeffrey S. Taube,et al.  Origins of landmark encoding in the brain , 2011, Trends in Neurosciences.

[42]  Jeffrey S. Taube,et al.  The vestibular contribution to the head direction signal and navigation , 2014, Front. Integr. Neurosci..

[43]  Verner P Bingman,et al.  Lateralized functional components of spatial cognition in the avian hippocampal formation: Evidence from single‐unit recordings in freely moving homing pigeons , 2006, Hippocampus.

[44]  D. Nitz,et al.  Spatial‐specificity of single‐units in the hippocampal formation of freely moving homing pigeons , 2005, Hippocampus.

[45]  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.

[46]  J. Taube,et al.  Firing Properties of Head Direction Cells in the Rat Anterior Thalamic Nucleus: Dependence on Vestibular Input , 1997, The Journal of Neuroscience.