Active maintenance of binocular correspondence leads to orientation alignment of visual receptive fields

Neural development in the visual cortex depends on the visual experience during the so-called critical period. Recent experiments have shown that under normal conditions rodents develop binocular receptive fields which have similar orientation preferences for the left and right eyes. In contrast, under conditions of monocular deprivation during the critical period, this orientation alignment does not happen. Here we propose a computational model to explain the process of orientation alignment, its underlying mechanisms, and its failure in case of monocular deprivation or uncorrelated binocular inputs. Our model is based on the recently proposed Active Efficient Coding framework that jointly develops eye movement control and sensory representations. Our model suggests that the active maintenance of a binocular visual field, which leads to correlated visual inputs from the two eyes, is essential for the process of orientation alignment. This behavior is analogous to vergence control in primates. However, due to the fact that rodents have large receptive fields with low spatial frequency tuning, the coordination of the eyes need not be very precise. The model also suggests that it is not necessary that coordinated binocular vision be maintained continuously in order for orientation alignment to develop.

[1]  Giulio Sandini,et al.  The iCub humanoid robot: an open platform for research in embodied cognition , 2008, PerMIS.

[2]  Jianhua Cang,et al.  Experience-dependent and independent binocular correspondence of receptive field subregions in mouse visual cortex. , 2014, Cerebral cortex.

[3]  Jianhua Cang,et al.  Critical Period Plasticity Matches Binocular Orientation Preference in the Visual Cortex , 2010, Neuron.

[4]  Stéphane Mallat,et al.  Matching pursuits with time-frequency dictionaries , 1993, IEEE Trans. Signal Process..

[5]  David S. Greenberg,et al.  Rats maintain an overhead binocular field at the expense of constant fusion , 2013, Nature.

[6]  Peter Dayan,et al.  Sparse Coding Can Predict Primary Visual Cortex Receptive Field Changes Induced by Abnormal Visual Input , 2013, PLoS Comput. Biol..

[7]  M. Frens,et al.  Three-dimensional optokinetic eye movements in the C57BL/6J mouse. , 2010, Investigative ophthalmology & visual science.

[8]  Shalabh Bhatnagar,et al.  Natural actor-critic algorithms , 2009, Autom..

[9]  Yu Zhao,et al.  Robust active binocular vision through intrinsically motivated learning , 2013, Front. Neurorobot..

[10]  Johannes Burge,et al.  Binocular integration and disparity selectivity in mouse primary visual cortex. , 2013, Journal of neurophysiology.

[11]  H. B. Barlow,et al.  Possible Principles Underlying the Transformations of Sensory Messages , 2012 .

[12]  L. Maffei,et al.  Visual depth perception in normal and deprived rats: Effects of environmental enrichment , 2013, Neuroscience.

[13]  Yu Zhao,et al.  A unified model of the joint development of disparity selectivity and vergence control , 2012, 2012 IEEE International Conference on Development and Learning and Epigenetic Robotics (ICDL).

[14]  Nishal P. Shah,et al.  Development and matching of binocular orientation preference in mouse V1 , 2014, Front. Syst. Neurosci..

[15]  J. Triesch,et al.  Power spectra of the natural input to the visual system , 2013, Vision Research.

[16]  M. Land Animal Vision: Rats Watch the Sky , 2013, Current Biology.

[17]  Markus Meister,et al.  Rats maintain a binocular field centered on the horizon , 2013, F1000Research.

[18]  David J. Field,et al.  Sparse coding with an overcomplete basis set: A strategy employed by V1? , 1997, Vision Research.

[19]  J. S Stahl,et al.  A comparison of video and magnetic search coil recordings of mouse eye movements , 2000, Journal of Neuroscience Methods.

[20]  David C. Knill,et al.  Orientation Disparity: A Cue for 3D Orientation? , 2009, Neural Computation.