Cross-species comparison of anticipatory and stimulus-driven neck muscle activity well before saccadic gaze shifts in humans and nonhuman primates

Abstract

Recent studies have described a phenomenon wherein the onset of a peripheral visual stimulus elicits short-latency (<100 ms) stimulus-locked recruitment (SLR) of neck muscles in nonhuman primates (NHPs), well before any saccadic gaze shift. The SLR is thought to arise from visual responses within the intermediate layers of the superior colliculus (SCi), hence neck muscle recordings may reflect presaccadic activity within the SCi, even in humans. We obtained bilateral intramuscular recordings from splenius capitis (SPL, an ipsilateral head-turning muscle) from 28 human subjects performing leftward or rightward visually guided eye-head gaze shifts. Evidence of an SLR was obtained in 16/55 (29%) of samples; we also observed examples where the SLR was present only unilaterally. We compared these human results with those recorded from a sample of eight NHPs from which recordings of both SPL and deeper suboccipital muscles were available. Using the same criteria, evidence of an SLR was obtained in 8/14 (57%) of SPL recordings, but in 26/29 (90%) of recordings from suboccipital muscles. Thus, both species-specific and muscle-specific factors contribute to the low SLR prevalence in human SPL. Regardless of the presence of the SLR, neck muscle activity in both human SPL and in NHPs became predictive of the reaction time of the ensuing saccade gaze shift ∼70 ms after target appearance; such pregaze recruitment likely reflects developing SCi activity, even if the tectoreticulospinal pathway does not reliably relay visually related activity to SPL in humans.

Stimulus-Locked Responses on Human Upper Limb Muscles and Corrective Reaches are Preferentially Evoked by Low Spatial Frequencies

“…4d, for the .56 versus 2.22 cpd 386 condition), obscuring the quantification of EMG recruitment attributable to the SLR. SLRs 387 tended to be easily distinguished at the lower but not higher SFs, as shown both by the vertical 388 banding tied to stimulus onset in trial-by-trial EMG activity, and a distinct initial peak or plateau 389 in the time-series ROC plots (see also Wood et al 2015). In contrast, time-series ROC plots for 390 higher SF stimuli, regardless of whether they were classified as SLR+ or SLR-, tended to lack a 391 clear initial peak or plateau after discrimination (e.g., 2 nd and 3 rd rows of Fig.…”

“…we performed this procedure in an attempt to isolate the effects of SF from perceived contrast, as 227 contrast influences SLR latency and magnitude (Wood et al, 2015). Second, perceptual contrast 228 matching mitigates some of the increases in RT with higher SFs (Breitmeyer, 1975), which was 229 important given that larger magnitude SLRs precede shorter RTs (Pruszynski et al, 2010; Gu et 230 al., 2016).…”

“…In each experiment, we used a single 236 standard stimulus presented at a suprathreshold 85% contrast from the middle SF used in each 237 experiment, with the comparison stimulus from each of the SFs being composed of a Gabor 238 patch presented at a higher or lower contrast, as determined by a staircase procedure. Our 239 rationale for using suprathreshold contrast is based on the relationship between SLR detectability 240 and contrast (Wood et al, 2015). After a reversal (participant changes response from increasing 241 to decreasing contrast or vice versa), the step size was decreased.…”

“…A value of .5 indicates chance discrimination, whereas values of 1 or 0 indicate 282 perfectly-correct or incorrect discrimination, respectively. Discrimination threshold was set to 283 0.6, which corresponds approximately to the upper 95% confidence interval determined using a 284 bootstrapping procedure (Goonetilleke et al, 2015). ROC latency was defined as the time where 285 the ROC time series surpassed threshold and remained above it for a minimum of eight out of ten 286…”

“…in EMG activity was more locked to stimulus onset than movement onset, for each SF we 294 performed a median-split of trials based on RT and conducted separate ROC time-series analyses 295 for both 'early RT' (i.e., the subset of shorter RT trials) and 'late RT' (the subset of longer RT 296 trials) subsets (Goonetilleke et al, 2015;Wood et al, 2015). We then calculated the slope of the 297 line connecting the average RT and the SLR latency for the 'early' and 'late' RT sub-groups (see 298 and vertical (90 degrees); a slope > 67.5 degrees indicates that EMG recruitment was more 301 locked to stimulus rather than movement onset.…”