Express saccades and superior colliculus responses are sensitive to short-wavelength cone contrast

Abstract

A key structure for directing saccadic eye movements is the superior colliculus (SC). The visual pathways that project to the SC have been reported to carry only luminance information and not color information. Short-wavelength-sensitive cones (S-cones) in the retina make little or no contribution to luminance signals, leading to the conclusion that S-cone stimuli should be invisible to SC neurons. The premise that S-cone stimuli are invisible to the SC has been used in numerous clinical and human psychophysical studies. The assumption that the SC cannot use S-cone stimuli to guide behavior has never been tested. We show here that express saccades, which depend on the SC, can be driven by S-cone input. Further, express saccade reaction times and changes in SC activity depend on the amount of S-cone contrast. These results demonstrate that the SC can use S-cone stimuli to guide behavior. We conclude that the use of S-cone stimuli is insufficient to isolate SC function in psychophysical and clinical studies of human subjects.S-cone | SC | macaque D ecades of oculomotor research have led to an incongruous conclusion: The oculomotor system does not use color information to guide the eyes (1, 2). However, it is natural to direct one's gaze to objects defined by color. Color vision in primates evolved because of the tremendous benefit of being able to discriminate colors and direct our actions accordingly (3, 4). The superior colliculus (SC) is a brainstem structure with a central role in the transformation of visual sensory signals into saccadic eye movements (2). Visual projections to the SC lack color opponent responses and appear to be dominated by luminance information (5-9). Luminance signals arise almost exclusively from long-and medium-wavelength-sensitive cones (L-and M-cones) in the retina, but not short-wavelength-sensitive cones (S-cones) (10). Instead, S-cones evolved to contribute to color vision (11). The takeaway is that the SC does not use color or S-cone input to guide saccades. This conclusion is surprising because both the SC and S-cones are evolutionarily ancient, and the SC has a central role in visually guided orienting behavior (2, 11).The proposition that the SC cannot detect S-cone stimuli has been leveraged to test SC function in diverse clinical and human psychophysical studies (12, 13). The scope of these investigations has ranged from mechanisms of blindsight (14-16), interhemispheric transfer in patients without a corpus callosum (17), face processing (18), and visual development (19) to inhibition of return (20), nasotemporal asymmetry (21), and the gap effect (22). The rationale for these experiments comes from an influential study by Sumner et al. (23), who noted that previous physiological and anatomical experiments had failed to find S-cone input to the SC. The idea is to present subjects with either a luminance or S-cone stimulus on separate trials of a visual or oculomotor task. If behavior [usually saccadic reaction time (RT)] is different in response to the S-cone stimulus, the ...

Fast saccadic and manual responses to faces presented to the koniocellular visual pathway

“…There was a significantly greater tendency to generate saccades to K-biased stimuli in the ∼200 msec time range than for corresponding P-biased (or M-biased) stimuli, as otherwise the K and P saccadic latency distributions are quite similar. Our findings are in agreement with the results of Hall and Colby (Hall & Colby, 2014;Hall & Colby, 2016) whereby K-biased stimuli were able to evoke activity in the macaque superior colliculus and the animals were able to generate short-latency saccades to such stimuli. The long latencies of sRTs evoked by M-biased stimuli are likely the result of having to resolve a small luminance contrast on rapidly changing (15 Hz) EEG background without the benefit of color opponency signals from either the K or P pathways.…”

“…However, saccade latencies in experiments employing simple low-luminance contrast stimuli (1°circular targets on black background) were as much as 150 msec longer than sRTs to brighter targets (Kveraga et al, 2002;Kveraga & Hughes, 2005). Therefore, it is not surprising that sRTs to M-biased face stimuli in the present study were much longer, especially given that we also employed a dynamic EEG background (Hall & Colby, 2014;Hall & Colby, 2016), which made stimuli with low luminance contrast more difficult to detect. Although Hall & Colby found sRTs to K targets to be on par with those to luminance targets, they used a much higher luminance contrast for the luminance targets (Hall & Colby, 2016).…”

Circuits for Action and Cognition: A View from the Superior Colliculus

“…Recent optogenetic studies show that there are also excitatory projections to the dorsal lateral geniculate nucleus (Bickford et al 2015). These new results, together with the known properties of retinal afferents and their recent molecular identification (Bowling & Michael 1980, Huberman et al 2009, Sachs & Schneider 1984, Tamamaki et al 1995), suggest the visuosensory layers process and relay visual information related to motion and orienting (Hall & Colby 2016, White et al 2009). Consistent with this, transneuronal retrograde labeling of collicular neurons after injections of rabies virus into extrastriate cortical areas shows that areas V3 and MT of the dorsal stream, but not areas V2 and V4 of the ventral stream, are targets of collicular outputs (Clower et al 2001, Lyon et al 2010).…”

TMS of V1 eliminates unconscious processing of chromatic stimuli

“…Although Tamietto et al (2010) have found an interesting dissociation between short and long wavelengths, the conclusion that their results reveal the RTE as mediated by the SC can be questioned. The possibility to eliminate SC activity using short-wavelength stimuli has been recently challenged because express saccades (fast saccades triggered by SC neurons) can be elicited by S-cone activating stimuli (Hall & Colby, 2016), and S-cone isolating stimuli can in fact activate the SC (Hall & Cloby, 2014). Another blindsight case shows an RTE produced by an unconscious achromatic redundant stimulus, but the RTE is absent for both unconscious S-cone activating stimuli and L- and M-cone activating stimuli (Marzi, Mancini, Metitieri, & Savazzi, 2009).…”