Estimation of self-motion duration and distance in rodents

Spatial orientation and navigation rely on information about landmarks and self-motion cues gained from multi-sensory sources. In this study, we focused on self-motion and examined the capability of rodents to extract and make use of information about own movement, i.e. path integration. Path integration has been investigated in depth in insects and humans. Demonstrations in rodents, however, mostly stem from experiments on heading direction; less is known about distance estimation. We introduce a novel behavioural paradigm that allows for probing temporal and spatial contributions to path integration. The paradigm is a bisection task comprising movement in a virtual reality environment in combination with either timing the duration ran or estimating the distance covered. We performed experiments with Mongolian gerbils and could show that the animals can keep track of time and distance during spatial navigation.

[1]  R. Wehner,et al.  The Ant Odometer: Stepping on Stilts and Stumps , 2006, Science.

[2]  John A. King,et al.  How vision and movement combine in the hippocampal place code , 2012, Proceedings of the National Academy of Sciences.

[3]  M. Goodale,et al.  A mammalian model of optic-flow utilization in the control of locomotion , 2004, Experimental Brain Research.

[4]  Joachim Hermann,et al.  Mongolian gerbils learn to navigate in complex virtual spaces , 2014, Behavioural Brain Research.

[5]  Georg B. Keller,et al.  Sensorimotor Mismatch Signals in Primary Visual Cortex of the Behaving Mouse , 2012, Neuron.

[6]  W. Meck,et al.  Journal of Experimental Psychology : General Ordinal Judgments in the Rat : An Understanding of Longer and Shorter for Suprasecond , but Not Subsecond , Durations , 2013 .

[7]  Benjamin J. Kraus,et al.  Hippocampal “Time Cells”: Time versus Path Integration , 2013, Neuron.

[8]  S. Lambert,et al.  Distance estimation in the hooded rat: Experimental evidence for the role of motion cues , 1990, Behavioural Brain Research.

[9]  Y. Dan,et al.  Representation of interval timing by temporally scalable firing patterns in rat prefrontal cortex , 2013, Proceedings of the National Academy of Sciences.

[10]  Yuji Naya,et al.  Context-dependent incremental timing cells in the primate hippocampus , 2014, Proceedings of the National Academy of Sciences.

[11]  Min Whan Jung,et al.  Neural Correlates of Interval Timing in Rodent Prefrontal Cortex , 2013, The Journal of Neuroscience.

[12]  Marcia Grabowecky,et al.  Simultaneous shape repulsion and global assimilation in the perception of aspect ratio. , 2011, Journal of vision.

[13]  Markus Lappe,et al.  Absolute travel distance from optic flow , 2005, Vision Research.

[14]  James G. Heys,et al.  The Functional Micro-organization of Grid Cells Revealed by Cellular-Resolution Imaging , 2014, Neuron.

[15]  Katherine R. Sherrill,et al.  Hippocampus and Retrosplenial Cortex Combine Path Integration Signals for Successful Navigation , 2013, The Journal of Neuroscience.

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

[17]  M. Shadlen,et al.  Representation of Time by Neurons in the Posterior Parietal Cortex of the Macaque , 2003, Neuron.

[18]  Colin Ellard,et al.  Visually guided locomotion and computation of time-to-collision in the Mongolian gerbil (Meriones unguiculatus): the effects of frontal and visual cortical lesions , 2000, Behavioural Brain Research.

[19]  Melvyn A. Goodale,et al.  Distance estimation in the mongolian gerbil: The role of dynamic depth cues , 1984, Behavioural Brain Research.

[20]  Thomas Wachtler,et al.  Contextual processing of brightness and color in Mongolian gerbils. , 2015, Journal of vision.

[21]  A. S. Etienne,et al.  Dead reckoning in a small mammal: the evaluation of distance , 1993, Journal of Comparative Physiology A.

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

[23]  Frank Jäkel,et al.  Bayesian inference for psychometric functions. , 2005, Journal of vision.

[24]  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.

[25]  A Schnee,et al.  Rats are able to navigate in virtual environments , 2005, Journal of Experimental Biology.

[26]  Zhang,et al.  Honeybee navigation en route to the goal: visual flight control and odometry , 1996, The Journal of experimental biology.

[27]  Rüdiger Wehner,et al.  Ant odometry in the third dimension , 2001, Nature.

[28]  Jonathan R. Whitlock,et al.  Navigating from hippocampus to parietal cortex , 2008, Proceedings of the National Academy of Sciences.

[29]  R. Church,et al.  Bisection of temporal intervals. , 1977, Journal of experimental psychology. Animal behavior processes.

[30]  Zhang,et al.  Visually mediated odometry in honeybees , 1997, The Journal of experimental biology.

[31]  Daoyun Ji,et al.  Activities of visual cortical and hippocampal neurons co-fluctuate in freely moving rats during spatial behavior , 2015, eLife.

[32]  M. Häusser,et al.  Cellular mechanisms of spatial navigation in the medial entorhinal cortex , 2013, Nature Neuroscience.

[33]  Ingo Fründ,et al.  Inference for psychometric functions in the presence of nonstationary behavior. , 2011, Journal of vision.

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

[35]  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.

[36]  Michael B. Reiser,et al.  Real neuroscience in virtual worlds , 2012, Current Opinion in Neurobiology.

[37]  Joseph J. Paton,et al.  A Scalable Population Code for Time in the Striatum , 2015, Current Biology.

[38]  M. Carandini,et al.  Integration of visual motion and locomotion in mouse visual cortex , 2013, Nature Neuroscience.

[39]  C. Büchel,et al.  Differential Recruitment of the Hippocampus, Medial Prefrontal Cortex, and the Human Motion Complex during Path Integration in Humans , 2007, The Journal of Neuroscience.

[40]  M V Srinivasan,et al.  Honeybee navigation: nature and calibration of the "odometer". , 2000, Science.

[41]  Christopher D. Harvey,et al.  Choice-specific sequences in parietal cortex during a virtual-navigation decision task , 2012, Nature.

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

[43]  Emilio Kropff,et al.  Place cells, grid cells, and the brain's spatial representation system. , 2008, Annual review of neuroscience.

[44]  Michael Jenkin,et al.  Humans can use optic flow to estimate distance of travel , 2001, Vision Research.

[45]  H. Eichenbaum,et al.  Hippocampal “Time Cells” Bridge the Gap in Memory for Discontiguous Events , 2011, Neuron.

[46]  E. Save,et al.  Dissociation of the effects of bilateral lesions of the dorsal hippocampus and parietal cortex on path integration in the rat. , 2001, Behavioral neuroscience.

[47]  Bruce L. McNaughton,et al.  Human Path Integration by Optic Flow , 2004, Spatial Cogn. Comput..

[48]  B. Johansson Chapter 25: Experimental models of altering the blood-brain barrier , 1992 .

[49]  John D. Aitchison,et al.  Optic Flow Input to the Hippocampal Formation from the Accessory Optic System , 1999, The Journal of Neuroscience.

[50]  Carlos D. Brody,et al.  Human performance on the temporal bisection task , 2010, Brain and Cognition.

[51]  F. Petzschner,et al.  Iterative Bayesian Estimation as an Explanation for Range and Regression Effects: A Study on Human Path Integration , 2011, The Journal of Neuroscience.

[52]  Ann M Graybiel,et al.  Neural representation of time in cortico-basal ganglia circuits , 2009, Proceedings of the National Academy of Sciences.

[53]  Ariane S Etienne,et al.  Path integration in mammals , 2004, Hippocampus.

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

[55]  Elizabeth R. Chrastil,et al.  Functional connections between optic flow areas and navigationally responsive brain regions during goal-directed navigation , 2015, NeuroImage.

[56]  Mary Hegarty,et al.  What determines our navigational abilities? , 2010, Trends in Cognitive Sciences.