Neural Mechanisms of Stimulus Velocity Tuning in the Superior Colliculus

Abstract

Superior colliculus (SC)-mediated control of visuomotor behavior depends on neuronal selectivity for stimulus velocity. However, the mechanism responsible for velocity tuning in SC neurons is unclear. It was shown in a previous study of anesthetized, decorticate hamsters that the number and distribution of feed-forward retinal inputs are not critical for velocity tuning. Here the alternate hypothesis that inhibition from the surround determines velocity tuning of SC neurons was tested. Surround inhibition was present in 65% (43/66) of SC neurons recorded in the superficial gray layer. Neurons within this group that were selective for slowly moving stimuli exhibited spatially asymmetric surround inhibition, and their velocity tuning arose by preferential suppression of responses to rapidly moving stimuli. In the other 35% (23/66) of SC neurons recorded, surround inhibition was weak or absent and did not play a role in velocity tuning. Most neurons with surround inhibition were nonselective for the duration of stationary flashed stimuli, whereas neurons without surround inhibition were selective for stimulus duration. The majority of neurons that preferred intermediate or rapidly moving stimuli exhibited spatially symmetric surround inhibition. In these neurons, occluding the surround reduced velocity selectivity by enhancing responses to slowly moving stimuli. Based on these data, a model is proposed suggesting spatiotemporal interactions between inhibition and excitation that could underlie velocity tuning.

Neural Mechanisms Underlying Selectivity for the Rate and Direction of Frequency-Modulated Sweeps in the Auditory Cortex of the Pallid Bat

“…It is not clear how these mechanisms can explain selectivity for fast velocities. However, in the visual layers of the superior colliculus, it has been suggested that a delayed inhibition from the RF surround may suppress responses to slow moving stimuli, but allow responses to fast moving stimuli (Razak and Pallas 2005). This is similar to observations in the pallid bat IC and cortex.…”

Altered cortical spectrotemporal processing with age-related hearing loss

“…Moreover, analogous to results with time expansion of consonants in audition, thresholds for detecting visual motion speed improve with increasing stimulus duration to a larger extent in older participants (Raghuram et al 2005). Similar receptive field mechanisms have been proposed to underlie FM rate selectivity and motion speed selectivity in auditory Fuzessery 2008, 2009;Trujillo et al 2013) and visual (Duysens et al 1985;Razak and Pallas 2005) systems, respectively. The similar deficits observed in the respective areas with aging are suggestive of similar underlying causes.…”

Facilitatory Mechanisms Underlying Selectivity for the Direction and Rate of Frequency Modulated Sweeps in the Auditory Cortex

“…Taken together, these studies suggest that there are at least three different mechanisms shaping FM sweep selectivity in the auditory system. In the mammalian visual system, similar mechanisms have been shown to shape movement direction and velocity selectivity (Goodwin and Henry, 1978; Movshon et al, 1978; Patel and Sillito, 1978; Duysens et al, 1985a,b; Jagadeesh et al, 1993; Livingstone, 1998; Murthy and Humphrey, 1999; Fried et al, 2005; Razak and Pallas, 2005). The difference appears to be in the relative extent to which each of these mechanisms contribute to selectivity in the different sensory systems.…”

“…For example, asymmetric sideband inhibition gives rise to direction and rate (velocity) selectivity in both visual (Goodwin and Henry, 1978; Patel and Sillito, 1978; Fried et al, 2005; Razak and Pallas, 2005) and auditory systems (Suga, 1965; Zhang et al, 2003; Fuzessery et al, 2006; Razak and Fuzessery, 2006). Similarly, selectivity for the duration a stimulus spends within the excitatory receptive field gives rise to rate selectivity in both the visual (Duysens et al, 1985a; 1985b) and auditory system (Fuzessery et al, 2006).…”