Eye movements and the maturation of cortical orientation selectivity

Neural activity appears to be a crucial component for shaping the receptive fields of cortical simple cells into adjacent, oriented subregions alternately receiving ON- and OFF-center excitatory geniculate inputs. It is known that the orientation selective responses of V1 neurons are refined by visual experience. After eye opening, the spatiotemporal structure of neural activity in the early stages of the visual pathway depends both on the visual environment and on how the environment is scanned. We have used computational modeling to investigate how eye movements might affect the refinement of the orientation tuning of simple cells in the presence of a Hebbian scheme of synaptic plasticity. Levels of correlation between the activity of simulated cells were examined while natural scenes were scanned so as to model sequences of saccades and fixational eye movements, such as microsaccades, tremor and ocular drift. The specific patterns of activity required for a quantitatively accurate development of simple cell receptive fields with segregated ON and OFF subregions were observed during fixational eye movements, but not in the presence of saccades or with static presentation of natural visual input. These results suggest an important role for the eye movements occurring during visual fixation in the refinement of orientation selectivity.

[1]  A Hein,et al.  Eye movements initiate visual-motor development in the cat. , 1979, Science.

[2]  M. Imbert,et al.  Ocular motility and recovery of orientational properties of visual cortical neurones in dark-reared kittens , 1978, Nature.

[3]  J. Malpeli,et al.  Effects of saccades on the activity of neurons in the cat lateral geniculate nucleus. , 1998, Journal of neurophysiology.

[4]  P. Buisseret,et al.  Influence of extraocular muscle proprioception on vision. , 1995, Physiological reviews.

[5]  P. Buisseret,et al.  Role of eye movements in developmental processes of orientation selectivity in the kitten visual cortex , 1986, Vision Research.

[6]  R D Freeman,et al.  Cortical plasticity in monocularly deprived immobilized kittens depends on eye movement. , 1979, Science.

[7]  D. Mastronarde Correlated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X- and Y-cells. , 1983, Journal of neurophysiology.

[8]  S. Sherman,et al.  Receptive-field characteristics of neurons in cat striate cortex: Changes with visual field eccentricity. , 1976, Journal of neurophysiology.

[9]  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.

[10]  M. Miyashita,et al.  A mathematical model for the self-organization of orientation columns in visual cortex. , 1992, Neuroreport.

[11]  G. DeAngelis,et al.  Spatiotemporal receptive field organization in the lateral geniculate nucleus of cats and kittens. , 1997, Journal of neurophysiology.