Synaptic noise is thought to be a limiting factor for computational efficiency in the brain. In visual cortex (V1), ongoing activity is present in vivo, and spiking responses to simple stimuli are highly unreliable across trials. Stimulus statistics used to plot receptive fields, however, are quite different from those experienced during natural visuomotor exploration. We recorded V1 neurons intracellularly in the anaesthetized and paralyzed cat and compared their spiking and synaptic responses to full field natural images animated by simulated eye-movements to those evoked by simpler (grating) or higher dimensionality statistics (dense noise). In most cells, natural scene animation was the only condition where high temporal precision (in the 10–20 ms range) was maintained during sparse and reliable activity. At the subthreshold level, irregular but highly reproducible membrane potential dynamics were observed, even during long (several 100 ms) “spike-less” periods. We showed that both the spatial structure of natural scenes and the temporal dynamics of eye-movements increase the signal-to-noise ratio by a non-linear amplification of the signal combined with a reduction of the subthreshold contextual noise. These data support the view that the sparsening and the time precision of the neural code in V1 may depend primarily on three factors: (1) broadband input spectrum: the bandwidth must be rich enough for recruiting optimally the diversity of spatial and time constants during recurrent processing; (2) tight temporal interplay of excitation and inhibition: conductance measurements demonstrate that natural scene statistics narrow selectively the duration of the spiking opportunity window during which the balance between excitation and inhibition changes transiently and reversibly; (3) signal energy in the lower frequency band: a minimal level of power is needed below 10 Hz to reach consistently the spiking threshold, a situation rarely reached with visual dense noise.

The computational role of primary visual cortex (V1) in low-level perception remains largely debated. A dominant view assumes the prevalence of higher cortical areas and top-down processes in binding information across the visual field. Here, we investigated the role of long-distance intracortical connections in form and motion processing by measuring, with intracellular recordings, their synaptic impact on neurons in area 17 (V1) of the anesthetized cat. By systematically mapping synaptic responses to stimuli presented in the nonspiking surround of V1 receptive fields, we provide the first quantitative characterization of the lateral functional connectivity kernel of V1 neurons. Our results revealed at the population level two structural-functional biases in the synaptic integration and dynamic association properties of V1 neurons. First, subthreshold responses to oriented stimuli flashed in isolation in the nonspiking surround exhibited a geometric organization around the preferred orientation axis mirroring the psychophysical "association field" for collinear contour perception. Second, apparent motion stimuli, for which horizontal and feedforward synaptic inputs summed in-phase, evoked dominantly facilitatory nonlinear interactions, specifically during centripetal collinear activation along the preferred orientation axis, at saccadic-like speeds. This spatiotemporal integration property, which could constitute the neural correlate of a human perceptual bias in speed detection, suggests that local (orientation) and global (motion) information is already linked within V1. We propose the existence of a "dynamic association field" in V1 neurons, whose spatial extent and anisotropy are transiently updated and reshaped as a function of changes in the retinal flow statistics imposed during natural oculomotor exploration.

ABSTRACT:Receptive