Abstract: Under natural viewing conditions, small movements of the eye, head and body prevent the maintenance of a steady direction of gaze. It is known that stimuli tend to fade when they are stabilized on the retina for several seconds. However, it is unclear whether the physiological motion of the retinal image serves a visual purpose during the brief periods of natural visual fixation. This study examines the impact of fixational instability on the statistics of the visual input to the retina and on the structure of neural activity in the early visual system. We show that fixational instability introduces a component in the retinal input signals that, in the presence of natural images, lacks spatial correlations. This component strongly influences neural activity in a model of the LGN. It decorrelates cell responses even if the contrast sensitivity functions of simulated cells are not perfectly tuned to counter-balance the power law spectrum of natural images. A decorrelation of neural activity at the early stages of the visual system has been proposed to be beneficial for discarding statistical redundancies in the input signals. The results of this study suggest that fixational instability might contribute to the establishment of efficient representations of natural stimuli.


[TOP]

Abstract: During visual fixation, small eye movements keep the retinal image continuously in motion. It is known that neurons in the visual system are sensitive to the spatiotemporal modulations of luminance resulting from this motion. In this study, we examined the influence of fixational eye movements on the statistics of neural activity in the macaque's retina during the brief intersaccadic periods of natural visual fixation. The responses of parvocellular (P) and magnocellular (M) ganglion cells in different regions of the visual field were modeled while their receptive fields scanned natural images following recorded traces of eye movements. Immediately after the onset of fixation, wide ensembles of coactive ganglion cells extended over several degrees of visual angle, both in the central and peripheral regions of the visual field. Following this initial pattern of activity, the covariance between the responses of pairs of P and M cells and the correlation between the responses of pairs of M cells dropped drastically during the course of fixation. Cell responses were completely uncorrelated by the end of a typical 300-ms fixation. This dynamic spatial decorrelation of retinal activity is a robust phenomenon independent of the specifics of the model. We show that it originates from the interaction of three factors: the statistics of natural scenes, the small amplitudes of fixational eye movements, and the temporal sensitivities of ganglion cells. These results support the hypothesis that fixational eye movements, by shaping the statistics of retinal activity, are an integral component of early visual representations.

[TOP]

Abstract: Under natural viewing conditions, the physiological instability of visual fixation keeps the projection of the stimulus on the retina in constant motion. After eye opening, chronic exposure to a constantly moving retinal image might influence the experience-dependent refinement of cell response characteristics. The results of previous modeling studies have suggested a contribution of fixational instability to the Hebbian maturation of the receptive fields of V1 simple cells (Rucci, Edelman, & Wray, 2000; Rucci&Casile, 2004). This letter examines the origins of such a contribution. Using quasilinear models of lateral geniculate nucleus units and V1 simple cells, we derive analytical expressions for the second order statistics of thalamocortical activity before and after eye opening. We show that in the presence of natural stimulation, fixational instability introduces a spatially uncorrelated signal in the retinal input, which strongly influences the structure of correlated activity in the model. This input signal produces a regime of thalamocortical activity similar to that present before eye opening and compatible with the
Hebbian maturation of cortical receptive fields.

[TOP]

Abstract: Early in life, visual experience appears to influence the refinement and maintenance of the orientation-selective responses of neurons in the primary visual cortex. After eye opening, the statistical structure of visually driven neural responses depends not only on the stimulus, but also on how the stimulus is scanned during behavior. Modulations of neural activity due to behavior may thus play a role in the experience-dependent refinement of cell response characteristics. To investigate the possible influences of eye movements on the maturation of thalamocortical connectivity, we have simulated the responses of neuronal populations in the lateral geniculate nucleus (LGN) and V1 of the cat while images of natural scenes were scanned in a way that replicated the cat's oculomotor activity. In the model, fixational eye movements were essential to attenuate neural sensitivity to the broad correlational structure of natural visual input, decorrelate neural responses, and establish a regime of neural activity that was compatible with a Hebbian segregation of geniculate afferents to the cortex. We show that this result is highly robust and does not depend on the precise characteristics of the model.


[TOP]

Abstract: Neural activity appears to be essential for the normal development of the orientation-selective responses of cortical cells. It has been proposed that the correlated activity of LGN cells is 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. After eye opening, the spatiotemporal structure of neural activity in the early stages of the visual pathway depends not only on the characteristics of the environment, but also on the way the environment is scanned. In this study, we use computational modeling to investigate how eye movements might affect the refinement of orientation tuning in the presence of a Hebbian scheme of synaptic plasticity. Visual input consisting of natural scenes scanned by varying types of eye movements was used to activate a spatiotemporal model of LGN cells. In the presence of different types of movement, significantly different patterns of activity were found in the LGN. Specific patterns of correlation required for the development of segregated cortical receptive field subregions were observed in the case of micromovements, but were not seen in the case of saccades or static presentation of natural visual input. These results suggest an important role for the eye movements occurring during fixation in the refinement of orientation selectivity.

[TOP]