Local Signals From Beyond the Receptive Fields of Striate Cortical Neurons

Abstract

Lennie. Local signals from beyond the receptive fields of striate cortical neurons. J Neurophysiol 90: 822-831, 2003. First published April 30, 2003 10.1152/jn.00005.2003. We examined in anesthetized macaque how the responses of a striate cortical neuron to patterns inside the receptive field were altered by surrounding patterns outside it. The changes in a neuron's response brought about by a surround are immediate and transient: they arise with the same latency as the response to a stimulus within the receptive field (this argues for a source locally in striate cortex) and become less effective as soon as 27 ms later. Surround signals appeared to exert their influence through divisive interaction (normalization) with those arising in the receptive field. Surrounding patterns presented at orientations slightly oblique to the preferred orientation consistently deformed orientation tuning curves of complex (but not simple) cells, repelling the preferred orientation but without decreasing the discriminability of the preferred grating and ones at slightly oblique orientations. By reducing responsivity and changing the tuning of complex cells locally in stimulus space, surrounding patterns reduce the correlations among responses of neurons to a particular stimulus, thus reducing the redundancy of image representation. I N T R O D U C T I O N"End-stopping" and "side-stopping" are well-known properties of receptive fields in striate cortex (V1) (Hubel and Wiesel 1965;Maffei and Fiorentini 1976). A pattern that extends beyond the receptive field often elicits a weaker response than a pattern that just fills it. This surrounding zone of inhibition is not generally considered part of the receptive field because stimuli falling on it cannot by themselves elicit a response. The most suppressive surrounding patterns usually have the same orientation and spatial frequency as those to which the receptive field is best tuned (Blakemore and Tobin 1972;Cavanaugh et al. 2002b;DeAngelis et al. 1994;Gilbert and Wiesel 1990;Levitt and Lund 1997;Nelson and Frost 1978;Sillito et al. 1995).It has been argued that the surround helps figure-ground segregation by suppressing signals within patches of uniform texture (Bradley and Andersen 1998;Lamme 1995;Sillito et al. 1995;Tanaka et al. 1986) and that it adjusts the responsivity of a neuron to the ambient contrast in the neighborhood of the receptive field (Cavanaugh et al. 2002a). We wondered if the surround might confer an additional benefit. In natural images, the correlation between the statistics of two regions declines with the separation of the regions (Simoncelli and Schwartz 1999). If a pattern falling on the surround consistently suppressed a neuron's response to a pattern of similar orientation falling on the receptive field, it might repel the neuron's orientation tuning curve, thereby reducing the correlation (redundancy) among visual signals that arise from adjacent image regions of similar structure. In this respect, the surround would act in the spatial domain in much the...

The Impact of Suppressive Surrounds on Chromatic Properties of Cortical Neurons

“…This is consistent with the idea that the signal of the surround is accumulated from a large pool of neurons with receptive fields in the region around the CRF (DeAngelis et al, 1994;Cavanaugh et al, 2002b;Müller et al, 2003). In V2, at least for those neurons that respond strongly to chromatic modulation, the surround has the same chromatic signature as the CRF and therefore exerts more powerful suppression when stimuli are modulated chromatically.…”

Early and Late Mechanisms of Surround Suppression in Striate Cortex of Macaque

“…The broadly tuned suppression does have the spatiotemporal signature of neurons in LGN and of neurons in the input layers of striate cortex (Blasdel and Fitzpatrick, 1984;Hawken et al, 1996). An early locus is also implied by the suppression being monocularly driven and is consistent with the observation (Bair et al, 2003;Müller et al, 2003) that some components of suppression are expressed as fast as the excitatory drive to the CRF. Surround suppression is already evident in LGN neurons (Solomon et al, 2002;Webb et al, 2005).…”

“…First, the action of the contrast gain control is firmly established as divisive, but it has been harder to establish that the surround acts in the same way (Sceniak et al, 2001;Cavanaugh et al, 2002a;Müller et al, 2003). To the extent that the two phenomena arise in the same mechanism, the action of the surround is more firmly established as divisive (Carandini et al, 1997).…”

Dynamics of Suppression in Macaque Primary Visual Cortex

“…If the same pool of inhibitory neurons were to underlie both types of suppression, their response properties should match, but this does not appear to be the case. Surround suppression is selective for the orientation and spatial frequency of the target in the surround (DeAngelis et al, 1994;Cavanaugh et al, 2002;Müller et al, 2003), whereas crossorientation suppression seems to lack selectivity (DeAngelis et al, 1992;Carandini et al, 1997). Our results show that the time courses of cross-orientation suppression and surround suppression are quite different.…”