Removal of inhibition uncovers latent movement potential during preparation

Abstract

33The motor system prepares for movements well in advance of their execution. In the gaze control system, 34 premotor neurons that produce a burst of activity for the movement are also active leading up to the 35 saccade. The dynamics of preparatory neural activity have been well described by stochastic accumulator 36 models, and variability in the accumulation dynamics has been shown to be correlated with reaction times 37 of the eventual saccade, but it is unclear whether this activity is purely preparatory in nature or has 38 features indicative of a hidden movement command. We explicitly tested whether preparatory neural 39 activity in premotor neurons of the primate superior colliculus has "motor potential". We removed 40 inhibition on the saccadic system using reflex blinks, which turn off downstream gating, and found that 41 saccades can be initiated before underlying activity reaches levels seen under normal conditions. 42Accumulating low-frequency activity was predictive of eye movement dynamics tens of milliseconds in 43 advance of the actual saccade, indicating the presence of a latent movement command. We also show that 44 reaching threshold is not a necessary condition for movement initiation, contrary to the postulates of 45 accumulation-to-threshold models. The results bring into question extant models of saccade generation 46 and support the possibility of a concurrent representation for movement preparation and generation. 47 Significance Statement 48How the brain plans for upcoming actions before deciding to initiate them is a central question in 49 neuroscience. Popular theories suggest that movement planning and execution occur in serial stages, 50 separated by a decision boundary in neural activity space (e.g., "threshold"), which needs to be crossed 51 before the movement is executed. By removing inhibitory gating on the motor system, we show here that 52 the activity required to initiate a saccade can be flexibly modulated. We also show that evolving activity 53 during movement planning is a hidden motor command. The results have important implications for our 54 understanding of how movements are generated, in addition to providing useful information for decoding 55 movement intention based on planning-related activity. 56

Instantaneous movement-unrelated midbrain activity modifies ongoing eye movements

“…3A) was similar to the timing of the SC visual bursts (Fig. 3B), showing a short lag of ~20 ms relative to the bursts that is consistent with an efferent processing delay from SC neurons to the final extraocular muscle drive (Jagadisan and Gandhi, 2017; Smalianchuk et al, 2018).…”

Motor selection dynamics in FEF explain the reaction time variance of saccades to single targets

“…Our results indicate that the threshold fluctuations are not random, but rather are coordinated with other elements of the circuitry, and although the proposed dynamics remain to be directly tested in other saccadic tasks, substantial agreement can already be found with extant data. For instance, movement-related activity preceding memory-guided saccades or anti-saccades is considerably weaker than for stimulus-driven saccades (Edelman and Goldberg, 2001), consistent with a lower threshold for internally-driven motor plans, and the same is true for saccades that are triggered by blinks (Jagadisan and Gandhi, 2017). The presaccadic activity measured during visual search is less vigorous for incorrect than for correct responses to the same location (Thompson et al, 2005), presumably because the former involve a stronger internal (and erroneous) drive that promotes a lower threshold.…”

“…According to the model, the saccadic threshold is not constant, but rather fluctuates quite dramatically. Such fluctuations are visible when comparing average movement-related activity across experimental conditions (Edelman and Goldberg, 2001; Thompson et al, 2005; Heitz and Schall, 2012; Jantz et al, 2013; Jagadisan and Gandhi, 2017) (Figs. 3, 5).…”

Time-course of population activity along the dorsoventral extent of the superior colliculus during delayed saccade tasks

“…Accordingly, across the active population, the neurons with the earliest buildup onset accumulate activity the longest and therefore have the highest firing rate at both burst onset and at peak. Given their saccade related discharge profiles, these are the putative neurons that project to the brainstem burst generator 54,55 and likely mediate instantaneous control of saccade velocity 56,57 . Further, the constant scaling factor between activity at burst onset to peak burst across channels (Figure 8) provides functional evidence of linear amplification in the motor burst 49 .…”