Otolith dysfunction alters exploratory movement in mice

Abstract The organization of rodent exploratory behavior appears to depend on self‐movement cue processing. As of yet, however, no studies have directly examined the vestibular system’s contribution to the organization of exploratory movement. The current study sequentially segmented open field behavior into progressions and stops in order to characterize differences in movement organization between control and otoconia‐deficient tilted mice under conditions with and without access to visual cues. Under completely dark conditions, tilted mice exhibited similar distance traveled and stop times overall, but had significantly more circuitous progressions, larger changes in heading between progressions, and less stable clustering of home bases, relative to control mice. In light conditions, control and tilted mice were similar on all measures except for the change in heading between progressions. This pattern of results is consistent with otoconia‐deficient tilted mice using visual cues to compensate for impaired self‐movement cue processing. This work provides the first empirical evidence that signals from the otolithic organs mediate the organization of exploratory behavior, based on a novel assessment of spatial orientation.

[1]  Derek A. Hamilton,et al.  Movement characteristics support a role for dead reckoning in organizing exploratory behavior , 2006, Animal Cognition.

[2]  I. Whishaw,et al.  Home bases formed to visual cues but not to self‐movement (dead reckoning) cues in exploring hippocampectomized rats , 2005, The European journal of neuroscience.

[3]  S. Besnard,et al.  Spatial and non-spatial performance in mutant mice devoid of otoliths , 2012, Neuroscience Letters.

[4]  Vikrant Kapoor,et al.  Mice Develop Efficient Strategies for Foraging and Navigation Using Complex Natural Stimuli , 2016, Current Biology.

[5]  M. Mintz,et al.  Mice with vestibular deficiency display hyperactivity, disorientation, and signs of anxiety , 2009, Behavioural Brain Research.

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

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

[8]  M. Ernst,et al.  Walking Straight into Circles , 2009, Current Biology.

[9]  David K Bilkey,et al.  Bilateral peripheral vestibular lesions produce long-term changes in spatial learning in the rat. , 2003, Journal of vestibular research : equilibrium & orientation.

[10]  Shawn S. Winter,et al.  The medial frontal cortex contributes to but does not organize rat exploratory behavior , 2016, Neuroscience.

[11]  Paul F. Smith,et al.  Locomotor and exploratory behavior in the rat following bilateral vestibular deafferentation. , 2008, Behavioral neuroscience.

[12]  Simon Benhamou,et al.  Spatial memory in large scale movements: Efficiency and limitation of the egocentric coding process , 1990 .

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

[14]  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.

[15]  Charles M Oman,et al.  Rat head direction cell responses in zero-gravity parabolic flight. , 2004, Journal of neurophysiology.

[16]  E. Batschelet Circular statistics in biology , 1981 .

[17]  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.

[18]  Jeffrey S. Taube,et al.  Disruption of the Head Direction Cell Signal after Occlusion of the Semicircular Canals in the Freely Moving Chinchilla , 2009, The Journal of Neuroscience.

[19]  D. Angelaki,et al.  Gravity orientation tuning in macaque anterior thalamus , 2016, Nature Neuroscience.

[20]  I. Whishaw,et al.  “Short‐stops” in rats with fimbria‐fornix lesions: Evidence for change in the mobility gradient , 1994, Hippocampus.

[21]  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.

[22]  M. Beraneck,et al.  Impaired perception of gravity leads to altered head direction signals: what can we learn from vestibular-deficient mice? , 2009, Journal of neurophysiology.

[23]  I. Whishaw,et al.  Fimbria-fornix lesions disrupt the dead reckoning (homing) component of exploratory behavior in mice. , 2002, Learning & memory.

[24]  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.

[25]  Jenny R. Köppen,et al.  Limbic system structures differentially contribute to exploratory trip organization of the rat , 2013, Hippocampus.

[26]  I. Whishaw,et al.  Hippocampectomized rats are impaired in homing by path integration , 1999, Hippocampus.

[27]  E. J. Green,et al.  Head-direction cells in the rat posterior cortex , 1994, Experimental Brain Research.

[28]  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.

[29]  A. A. Schaeffer,et al.  Spiral movement in man , 1928 .

[30]  Benjamin J. Clark,et al.  Motor activity (exploration) and formation of home bases in mice (C57BL/6) influenced by visual and tactile cues: Modification of movement distribution, distance, location, and speed , 2006, Physiology & Behavior.

[31]  D. Eilam,et al.  Home base behavior of rats (Rattus norvegicus) exploring a novel environment , 1989, Behavioural Brain Research.

[32]  J. Taube,et al.  Head direction cell activity monitored in a novel environment and during a cue conflict situation. , 1995, Journal of neurophysiology.

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

[34]  J. O’Keefe,et al.  Hippocampal place units in the freely moving rat: Why they fire where they fire , 1978, Experimental Brain Research.

[35]  M. P. McDonald,et al.  Endogenous anxiety and stress responses in water maze and Barnes maze spatial memory tasks , 2009, Behavioural Brain Research.

[36]  Ofer Tchernichovski,et al.  A phase plane representation of rat exploratory behavior , 1995, Journal of Neuroscience Methods.

[37]  Douglas G. Wallace,et al.  Medial septum lesions disrupt exploratory trip organization: Evidence for septohippocampal involvement in dead reckoning , 2007, Physiology & Behavior.

[38]  H. Mittelstaedt,et al.  Homing by path integration in a mammal , 1980, Naturwissenschaften.

[39]  I. Whishaw,et al.  NMDA lesions of Ammon's horn and the dentate gyrus disrupt the direct and temporally paced homing displayed by rats exploring a novel environment: evidence for a role of the hippocampus in dead reckoning , 2003, The European journal of neuroscience.

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

[41]  A. Etienne,et al.  Navigation through vector addition , 1998, Nature.

[42]  Benjamin J. Clark,et al.  Movements of exploration intact in rats with hippocampal lesions , 2005, Behavioural Brain Research.

[43]  J. Taube,et al.  Degradation of Head Direction Cell Activity during Inverted Locomotion , 2005, The Journal of Neuroscience.

[44]  R. Stackman,et al.  Rats with lesions of the vestibular system require a visual landmark for spatial navigation , 2002, Behavioural Brain Research.

[45]  Gregor Schöner,et al.  Neural dynamics parametrically controlled by image correlations organize robot navigation , 1996, SNN Symposium on Neural Networks.

[46]  Stefan Glasauer,et al.  Idiothetic navigation in Gerbils and Humans , 1991 .

[47]  B. J. Clark,et al.  Both visual and idiothetic cues contribute to head direction cell stability during navigation along complex routes. , 2011, Journal of neurophysiology.

[48]  C. Vorhees,et al.  Morris water maze: procedures for assessing spatial and related forms of learning and memory , 2006, Nature Protocols.

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

[50]  David Eilam,et al.  Stopping behavior: constraints on exploration in rats (Rattus norvegicus) , 1993, Behavioural Brain Research.

[51]  Jenny R. Köppen,et al.  Infusion of GAT1-saporin into the medial septum/vertical limb of the diagonal band disrupts self-movement cue processing and spares mnemonic function , 2013, Brain Structure and Function.

[52]  Jenny R. Köppen,et al.  Cholinergic deafferentation of the hippocampus causes non-temporally graded retrograde amnesia in an odor discrimination task , 2016, Behavioural Brain Research.

[53]  D. Wallace,et al.  Selective hippocampal cholinergic deafferentation impairs self-movement cue use during a food hoarding task , 2007, Behavioural Brain Research.

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

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

[56]  C. Gallistel The organization of learning , 1990 .

[57]  Douglas G. Wallace,et al.  Fractionating dead reckoning: role of the compass, odometer, logbook, and home base establishment in spatial orientation , 2008, Naturwissenschaften.

[58]  Stephane Valerio,et al.  Head Direction Cell Activity Is Absent in Mice without the Horizontal Semicircular Canals , 2016, The Journal of Neuroscience.