Modeling Boundary Vector Cell Firing Given Optic Flow as a Cue

Boundary vector cells in entorhinal cortex fire when a rat is in locations at a specific distance from walls of an environment. This firing may originate from memory of the barrier location combined with path integration, or the firing may depend upon the apparent visual input image stream. The modeling work presented here investigates the role of optic flow, the apparent change of patterns of light on the retina, as input for boundary vector cell firing. Analytical spherical flow is used by a template model to segment walls from the ground, to estimate self-motion and the distance and allocentric direction of walls, and to detect drop-offs. Distance estimates of walls in an empty circular or rectangular box have a mean error of less than or equal to two centimeters. Integrating these estimates into a visually driven boundary vector cell model leads to the firing patterns characteristic for boundary vector cells. This suggests that optic flow can influence the firing of boundary vector cells.

[1]  J A Perrone,et al.  Model for the computation of self-motion in biological systems. , 1992, Journal of the Optical Society of America. A, Optics and image science.

[2]  Robert C. Bolles,et al.  Random sample consensus: a paradigm for model fitting with applications to image analysis and automated cartography , 1981, CACM.

[3]  William H. Warren,et al.  Optic flow is used to control human walking , 2001, Nature Neuroscience.

[4]  A. Burkhalter,et al.  Hierarchical organization of areas in rat visual cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  Mark P. Brandon,et al.  Reduction of Theta Rhythm Dissociates Grid Cell Spatial Periodicity from Directional Tuning , 2011, Science.

[6]  P. Best,et al.  Spatial processing in the brain: the activity of hippocampal place cells. , 2001, Annual review of neuroscience.

[7]  Markus Lappe,et al.  A model of the combination of optic flow and extraretinal eye movement signals in primate extrastriate visual cortex: Neural model of self-motion from optic flow and extraretinal cues , 1998, Neural Networks.

[8]  E. Marg THE ACCESSORY OPTIC SYSTEM * , 1964 .

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

[10]  J. W. Humberston Classical mechanics , 1980, Nature.

[11]  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.

[12]  C. Barry,et al.  Learning in a geometric model of place cell firing , 2007, Hippocampus.

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

[14]  K. Jeffery,et al.  Learned interaction of visual and idiothetic cues in the control of place field orientation , 1999, Experimental Brain Research.

[15]  J H Rieger,et al.  Information in optical flows induced by curved paths of observation. , 1983, Journal of the Optical Society of America.

[16]  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.

[17]  Stephen P. Boyd,et al.  Convex Optimization , 2004, Algorithms and Theory of Computation Handbook.

[18]  Florentin Wörgötter,et al.  Statistics of optic flow for self-motion through natural scenes , 2004 .

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

[20]  C. Duffy MST neurons respond to optic flow and translational movement. , 1998, Journal of neurophysiology.

[21]  M. Graziano,et al.  Tuning of MST neurons to spiral motions , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  R. Wurtz,et al.  Response of monkey MST neurons to optic flow stimuli with shifted centers of motion , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  P. Best,et al.  Spatial correlates of hippocampal unit activity are altered by lesions of the fornix and entorhinal cortex , 1980, Brain Research.

[24]  J. G. Parnavelas,et al.  Response properties of neurons in the visual cortex of the rat , 2004, Experimental Brain Research.

[25]  J. Knierim,et al.  Influence of boundary removal on the spatial representations of the medial entorhinal cortex , 2008, Hippocampus.

[26]  Ashley N. Linder,et al.  The Spatial Periodicity of Grid Cells Is Not Sustained During Reduced Theta Oscillations , 2011, Science.

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

[28]  J O'Keefe,et al.  Robotic and neuronal simulation of the hippocampus and rat navigation. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[29]  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.

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

[31]  Constance S. Royden,et al.  Mathematical analysis of motion-opponent mechanisms used in the determination of heading and depth. , 1997, Journal of the Optical Society of America. A, Optics, image science, and vision.

[32]  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.

[33]  J. O’Keefe,et al.  Modeling place fields in terms of the cortical inputs to the hippocampus , 2000, Hippocampus.

[34]  A Routtenberg,et al.  Kainic acid induction of mossy fiber sprouting: Dependence on mouse strain , 2000, Hippocampus.

[35]  B. J. Yates,et al.  Does the vestibular system contribute to head direction cell activity in the rat? , 2002, Physiology & Behavior.

[36]  K. Jeffery,et al.  The Boundary Vector Cell Model of Place Cell Firing and Spatial Memory , 2006, Reviews in the neurosciences.

[37]  Torkel Hafting,et al.  Conjunctive Representation of Position, Direction, and Velocity in Entorhinal Cortex , 2006, Science.

[38]  A. J. Hill,et al.  Effects of deafness and blindness on the spatial correlates of hippocampal unit activity in the rat , 1981, Experimental Neurology.

[39]  K. Tanaka,et al.  Analysis of motion of the visual field by direction, expansion/contraction, and rotation cells clustered in the dorsal part of the medial superior temporal area of the macaque monkey. , 1989, Journal of neurophysiology.

[40]  B. McNaughton,et al.  Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. , 1998, Journal of neurophysiology.

[41]  R. Lund,et al.  Receptive field properties of single neurons in rat primary visual cortex. , 1999, Journal of neurophysiology.

[42]  Michael E. Hasselmo,et al.  Modeling the influence of optic flow on grid cell firing in the absence of other cues1 , 2012, Journal of Computational Neuroscience.

[43]  J. Perrone,et al.  A model of self-motion estimation within primate extrastriate visual cortex , 1994, Vision Research.

[44]  D. Rubin,et al.  Maximum likelihood from incomplete data via the EM - algorithm plus discussions on the paper , 1977 .

[45]  J. O’Keefe,et al.  Boundary Vector Cells in the Subiculum of the Hippocampal Formation , 2009, The Journal of Neuroscience.

[46]  Markus Lappe,et al.  A Neural Network for the Processing of Optic Flow from Ego-Motion in Man and Higher Mammals , 1993, Neural Computation.

[47]  H. C. Longuet-Higgins,et al.  The interpretation of a moving retinal image , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

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