Neural mechanisms underlying the temporal control of sequential saccade planning in the frontal eye fields

Abstract

SummaryA ramp to threshold activity of frontal Eye Field (FEF) movement-related neurons best explains the reaction time of single saccades. How such activity is modulated by a concurrent saccade plan is not known. Borrowing from psychological theories of capacity sharing that are designed to explain the concurrent planning of two decisions, we show that processing bottlenecks are brought about by decreasing the growth rate and increasing the threshold of saccade-related activity. Further, rate perturbation affects both saccade plans, indicating a capacity-sharing mechanism of processing bottlenecks, where both the saccade plans compete for processing capacity. To understand how capacity sharing was neurally instantiated, we designed a model in which movement fields that instantiate two saccade plans, mutually inhibit each other. In addition to predicting the greater reaction times for both saccades and changes in growth rate and threshold activity observed experimentally, we observed a greater separation of the two neural trajectories in neural state space, which was verified experimentally. Finally, we show that in contrast to movement related neurons, visual activity in FEF neurons are not affected by the presence of multiple saccade targets, indicating that inhibition amongst movement-related neurons instantiates capacity sharing. Taken together, we show how psychology-inspired models of capacity sharing can be mapped onto neural responses to understand the control of rapid saccade sequences.

Neck motor unit activity displays neural signatures of temporal control during sequential saccade planning

“…Consistent with the results obtained from the FEF movement neuron activity (Basu et al, 2021), rate perturbation was present even when the first saccade went into the response field ( Fig. 4D-E ; Wilcoxon signed-rank test, Z = -3.54, p < .0001).…”

“…Baseline and onset of activity did not distinguish between the target step delays across the population ( p > .05). The changes in these parameters reflected the population dynamics seen at the FEF level (Basu et al, 2021; Fig. 4C ).…”

“…Before checking EMG responses for sequential saccades, we checked the EMG responses for single saccades in the no-step trials. Corroborating with the rise-to-threshold hypothesis of accumulator models (Hanes and Schall, 1996), FEF movement neuron activity altered the rate of growth but not the threshold to account for reaction time variability in the single saccade no-step trials (Basu et al, 2021). The EMG activity showed similar profiles, ramping up activity in an accumulator framework, with the rate of growth on an average, being greater in trials with faster reaction times (one-way ANOVA, F (1, 123) = 12.89, p < .001).…”

“…S2 ). In our previous study, we have shown that these longer response times reflect the activity of FEF responses which slows down when two closely-spaced saccade plans proceed simultaneously (Basu et al, 2021).…”

“…We have previously shown that a sequence of two saccades may be programmed in parallel in the FEF, albeit with processing limitations ( Fig. 1B ; Basu et al, 2021; Basu and Murthy, 2020). The transfer of concurrent saccade programming signals from FEF to neck muscle may be inhibited to prevent premature head motion for second gaze shift while the first gaze plan is still underway.…”