Development and Binocular Matching of Orientation Selectivity in Visual Cortex: A Computational Model.

In mouse visual cortex, right after eye-opening binocular cells have different preferred orientations for input from the two eyes. With normal visual experience during a critical period, these preferred orientations evolve and eventually become well matched. To gain insight into the matching process, we developed a computational model of a cortical cell receiving orientation selective inputs via plastic synapses.The model captures the experimentally observed matching of the preferred orientations, the dependence of matching on ocular dominance of the cell, and the relationship between the degree of matching and the resulting monocular orientation selectivity. Moreover, our model puts forward testable predictions: i) The matching speed increases with initial ocular dominance; ii) While the matching improves more slowly for cells that are more orientation-selective, the selectivity increases faster for better matched cells during the matching process. This suggests that matching drives orientation selectivity but not vice versa; iii) there are two main routes to matching: the preferred orientations either drift towards each other or one of the orientations switches suddenly. The latter occurs for cells with large initial mismatch and can render the cells monocular. We expect that these results provide insight more generally into the development of neuronal systems that integrate inputs from multiple sources, including different sensory modalities.

[1]  K. Miller,et al.  Ocular dominance column development: analysis and simulation. , 1989, Science.

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

[3]  Gerald J. Sun,et al.  Persistent Structural Plasticity Optimizes Sensory Information Processing in the Olfactory Bulb , 2016, Neuron.

[4]  W. Gerstner,et al.  Dynamic I-V curves are reliable predictors of naturalistic pyramidal-neuron voltage traces. , 2008, Journal of neurophysiology.

[5]  R. Reid,et al.  Homeostatic Regulation of Eye-Specific Responses in Visual Cortex during Ocular Dominance Plasticity , 2007, Neuron.

[6]  E. Knudsen,et al.  Sensitive Periods for Visual Calibration of the Auditory Space Map in the Barn Owl Optic Tectum , 1998, The Journal of Neuroscience.

[7]  Jianhua Cang,et al.  Sublinear Binocular Integration Preserves Orientation Selectivity in Mouse Visual Cortex , 2013, Nature Communications.

[8]  M. Wallace,et al.  Converging influences from visual, auditory, and somatosensory cortices onto output neurons of the superior colliculus. , 1993, Journal of neurophysiology.

[9]  Marla B. Feller,et al.  Spatiotemporal Features of Retinal Waves Instruct the Wiring of the Visual Circuitry , 2016, Front. Neural Circuits.

[10]  Jianhua Cang,et al.  Environmental Enrichment Rescues Binocular Matching of Orientation Preference in Mice that Have a Precocious Critical Period , 2013, Neuron.

[11]  M. Stryker,et al.  The role of visual experience in the development of columns in cat visual cortex. , 1998, Science.

[12]  L. Cooper,et al.  Synaptic plasticity in visual cortex: comparison of theory with experiment. , 1991, Journal of neurophysiology.

[13]  D. Hansel,et al.  The Mechanism of Orientation Selectivity in Primary Visual Cortex without a Functional Map , 2012, The Journal of Neuroscience.

[14]  KD Miller A model for the development of simple cell receptive fields and the ordered arrangement of orientation columns through activity-dependent competition between ON- and OFF-center inputs , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  Nicholas J. Priebe,et al.  Emergent Orientation Selectivity from Random Networks in Mouse Visual Cortex , 2018, bioRxiv.

[16]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[17]  V. Mountcastle The columnar organization of the neocortex. , 1997, Brain : a journal of neurology.

[18]  Kenichi Ohki,et al.  Neuronal activity is not required for the initial formation and maturation of visual selectivity , 2015, Nature Neuroscience.

[19]  M P Stryker,et al.  Experience-Dependent Plasticity of Binocular Responses in the Primary Visual Cortex of the Mouse , 1996, The Journal of Neuroscience.

[20]  Helge J. Ritter,et al.  The Joint Development of Orientation and Ocular Dominance: Role of Constraints , 1997, Neural Computation.

[21]  M. Stryker,et al.  Development of orientation selectivity in ferret visual cortex and effects of deprivation , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  J. K. Harting,et al.  Connectional organization of the superior colliculus , 1984, Trends in Neurosciences.

[23]  Benjamin A Rowland,et al.  Organization and plasticity in multisensory integration: early and late experience affects its governing principles. , 2011, Progress in brain research.

[24]  M. Stryker,et al.  Development and Plasticity of the Primary Visual Cortex , 2012, Neuron.

[25]  E. Bienenstock,et al.  Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  K. Miller,et al.  A Theory of the Transition to Critical Period Plasticity: Inhibition Selectively Suppresses Spontaneous Activity , 2013, Neuron.

[27]  C. Niell,et al.  Layer-Specific Refinement of Visual Cortex Function after Eye Opening in the Awake Mouse , 2015, The Journal of Neuroscience.

[28]  Hui Chen,et al.  Environmental Enrichment Rescues Binocular Matching of Orientation Preference in the Mouse Visual Cortex , 2017, The Journal of Neuroscience.

[29]  W. M. Keck,et al.  Highly Selective Receptive Fields in Mouse Visual Cortex , 2008, The Journal of Neuroscience.

[30]  K. Miller,et al.  Correlation-Based Development of Ocularly Matched Orientation and Ocular Dominance Maps: Determination of Required Input Activities , 1998, The Journal of Neuroscience.

[31]  Wulfram Gerstner,et al.  Adaptive exponential integrate-and-fire model as an effective description of neuronal activity. , 2005, Journal of neurophysiology.

[32]  W. Gerstner,et al.  Connectivity reflects coding: a model of voltage-based STDP with homeostasis , 2010, Nature Neuroscience.

[33]  John G McHaffie,et al.  Axon morphologies and convergence patterns of projections from different sensory-specific cortices of the anterior ectosylvian sulcus onto multisensory neurons in the cat superior colliculus. , 2009, Cerebral cortex.

[34]  M. Fagiolini,et al.  Inhibitory threshold for critical-period activation in primary visual cortex , 2000, Nature.