Saccadic Inhibition Reveals the Timing of Automatic and Voluntary Signals in the Human Brain

Abstract

Neurophysiological and phenomenological data on sensorimotor decision making are growing so rapidly that it is now necessary and achievable to capture it in biologically inspired models, for advancing our understanding in both research and clinical settings. However, the main impediment in moving from elegant models with few free parameters to more complex biological models in humans lies in constraining the more numerous parameters with behavioral data (without human single-cell recording). Here we show that a behavioral effect called "saccadic inhibition" (1) is predicted by existing complex (neuronal field) models, (2) constrains crucial temporal parameters of the model, precisely enough to address individual differences, and (3) is not accounted for by current simple decision models, even after significant additions. Visual onsets appearing while an observer plans a saccade knock out a subpopulation of saccadic latencies that would otherwise occur, producing a clear dip in the latency distribution. This overlooked phenomenon is remarkably well time locked across conditions and observers, revealing and characterizing a fast automatic component of visual input to oculomotor competition. The neural field model not only captures this but predicts additional features that are borne out: the dips show spatial specificity, are lawfully modulated in contrast, and occur with S-cone stimuli invisible to the retinotectal route. Overall, we provide a way forward for applying precise neurophysiological models of saccade planning in humans at the individual level.

Competitive Integration of Visual and Goal-related Signals on Neuronal Accumulation Rate: A Correlate of Oculomotor Capture in the Superior Colliculus

“…This is in line with the hypothesis that the nonoverlapping visual and goalrelated signals associated with this condition were mutually inhibitory ( Figure 1C), thereby suppressing baseline activation away from saccade threshold. This latter result is also consistent with human studies on the effect of remote distractors (McSorley, McCloy, & Lyne, 2012;Bompas & Sumner, 2011;Born & Kerzel, 2011;White, Gegenfurtner, & Kerzel, 2005;Walker, Deubel, Schneider, & Findlay, 1997).…”

“…Neurophysiological support for this has been found in the FEFs (Purcell, Schall, Logan, & Palmeri, 2012; and the SC (Paré & Hanes, 2003; see also Basso & Wurtz, 1997). Computational models of the SCi have extended this idea by examining the spatial interaction between visual and goal-related signals within a dynamic competitive framework (Marino, Trappenberg, et al, 2012;Bompas & Sumner, 2011;Meeter et al, 2010;Godijn & Theeuwes, 2002;Trappenberg et al, 2001). An assumption underlying these models is that visual and goal-related signals mutually inhibit or excite one another depending on the spatial proximity of their corresponding population responses or "point images" (Marino, Rodgers, Levy, & Munoz, 2008;McIlwain, 1986); that is, the local population of neurons activated by a given stimulus (see Methods).…”

“…There is evidence supported by several biologically inspired models that the superior colliculus (SC) plays an important role in resolving competitive interactions between visual and goal-related processes (Marino, Trappenberg, Dorris, & Munoz, 2012;Bompas & Sumner, 2011;Meeter, Van der Stigchel, & Theeuwes, 2010;Dorris, Olivier, & Munoz, 2007;Godijn & Theeuwes, 2002;Trappenberg, Dorris, Munoz, & Klein, 2001). Neurons in the superficial SC layers (SCs) receive input predominantly from the retina and visual cortex, whereas neurons in the intermediate SC layers (SCi) integrate multisensory, cognitive, and motor information from several cortical and subcortical brain areas (see White & Munoz, 2011b, for a recent review).…”

Impairment of manual but not saccadic response inhibition following acute alcohol intoxication

“…Eye movement data was processed following standard procedures (e.g., Bompas and Sumner, 2011). Briefly, accepted saccades were detected using a velocity criterion of greater than 35°/s, an acceleration of 6000°/s2 trials, and an amplitude of at least 6°(halfway to the target).…”

“…Latency distributions from both saccades and manual responses on signal-present ignore trials were analysed for the presence, amplitude and delay of 'dips' time-locked to the onset of the signal following the procedure detailed in Bompas and Sumner (2011). In order to provide enough trials to generate good quality saccade latency distributions, data were pooled across all participants and statistical tests were not able to be conducted.…”