Input-Gain Control Produces Feature-Specific Surround Suppression

Abstract

In primary visual cortex (V1), neuronal responses are sensitive to context. For example, responses to stimuli presented within the receptive field (RF) center are often suppressed by stimuli within the RF surround, and this suppression tends to be strongest when the center and surround stimuli match. We sought to identify the mechanism that gives rise to these properties of surround modulation. To do so, we exploited the stability of implanted multielectrode arrays to record from neurons in V1 of alert monkeys with multiple stimulus sets that more exhaustively probed center-surround interactions. We first replicated previous results concerning center-surround similarity using gratings representing all combinations of center and surround orientation. With this stimulus set, the surround simply scaled population responses to the center, such that the overall population tuning curve had the same shape and peak response. However, when the center contained two superimposed gratings (i.e., a visual "plaid"), one component of which always matched the surround orientation, suppression selectively affected the portion of the response driven by the matching center component, thereby producing shifts in the peak of the population orientation tuning curve. In effect, the surround caused neurons to respond predominantly to the component grating of the center plaid that was unmatched to the surround grating, as if by reducing the effective strength of whichever stimulus attributes were matched to the surround. These results provide key physiological support for theoretical models that propose feature-specific, input-gain control as the mechanism underlying surround suppression.

Distinct spatiotemporal mechanisms underlie extra-classical receptive field modulation in macaque V1 microcircuits

“…With this biphasic temporal profile, integration of the spiking response over short epochs yields facilitation compared to CRF stimulation alone ( Figure 6) as observed by Kapadia et al (2000). Integration of the response over longer stimulus durations leads to net measured suppression as the stronger, delayed suppressive component dominates over facilitation (Figure 6), as reported in many studies (Jones et al, 2001;Sceniak et al, 2001;Cavanaugh et al, 2002b;Webb et al, 2005;Hallum and Movshon, 2014;Trott and Born, 2015). We suggest that these differences in temporal integration among multiple eCRF components provide a parsimonious explanation for many previous conflicting reports about eCRF facilitation (and lack thereof).…”

“…Studies of eCRF modulation that used large collinear annular gratings drifting for hundreds of milliseconds to many seconds typically reported finding strong eCRF collinear suppression but little or no collinear facilitation (Levitt and Lund, 1997;Hupe et al, 2001;Sceniak et al, 2001;Levitt and Lund, 2002;Cavanaugh et al, 2002a;Jones et al, 2002;Shushruth et al, 2012;Nassi et al, 2013;Henry et al, 2013;Trott and Born, 2015). Other studies, that used briefly presented spatially-localized stimuli flanking the CRF (Kapadia et al, 1995;Kapadia et al, 2000), reported a high prevalence of collinear facilitation.…”

Spatial contextual effects in primary visual cortex limit feature representation under crowding

“…Similarly, the crowding effects we measured are not influenced by eye movements, since we administered paralytics to suppress these. Importantly, V1 spatial contextual effects are robust in awake animals, and have similar properties to the modulation observed under anesthesia 64,65 .…”

Cortico-cortical feedback from V2 exerts a powerful influence over the visually evoked local field potential and associated spike timing in V1

“…The experimental details have been described previously (Nassi et al, 2013;Trott and Born, 2015). Briefly, two male rhesus monkeys (Macaca mulatta), A and U, were implanted with a head post, a multi-electrode array (MEA) over the V1 operculum, and three custom made cryoloops (Lomber et al, 1999) into the lunate sulcus in an aseptic surgery under isoflurane anesthesia.…”