Mechanisms that allow cortical preparatory activity without inappropriate movement

Abstract

32We reveal a novel mechanism that explains how preparatory activity can evolve in motor-related 33 cortical areas without prematurely inducing movement. The smooth eye movement region of the 34 frontal eye fields (FEFSEM) is a critical node in the neural circuit controlling smooth pursuit eye 35 movement. Preparatory activity evolves in FEFSEM during fixation in parallel with an objective 36 measure of visual-motor gain. We propose that the use of FEFSEM output as a gain signal 37 allows for preparation to progress in the pursuit system without causing movement. We also 38 show that preparatory modulation of firing rate in FEFSEM progresses in a way that predicts 39 movement, providing evidence against the "movement-null" space hypothesis of how 40 preparatory activity can progress without movement. Finally, there is partial reorganization of 41 FEFSEM population activity between preparation and movement. We propose that this 42 reorganization allows for a directionally non-specific component of preparatory visual-motor 43 gain enhancement in the pursuit system. 44 83of an all-or-none inhibitory gate created by the action of omnipause neurons in the brainstem 84 (Cohen and Henn, 1972; Keller, 1974a; Luschei and Fuchs, 1972). Ramps of preparatory activity 85 in the saccadic region of the frontal eye fields fail to trigger eye movements until the collective 86 descending activity from the frontal eye fields and superior colliculus cause the omnipause 87 4 neurons to cease firing, releasing the circuits that generate movement (Dorris et al., 1997; Hanes 88 and Schall, 1996). However, there is no evidence that pursuit system uses the all-or-none gate 89 that controls saccades (Missal and Keller, 2002; Schwartz and Lisberger, 1994). 90Here we propose a third, different, mechanism for movement prevention during motor 91 preparation. The outputs from the FEFSEM seem to control the gain of visual-motor transmission 92 for pursuit (Nuding et al., 2009; Tanaka and Lisberger, 2001). Further, visual-motor gain is 93 dialed up in preparation for an imminent smooth eye movement (Kodaka and Kawano, 2003; 94 Tabata et al., 2006). In the present paper, we show striking parallels between the progression of 95 preparatory activity in FEFSEM and the preparatory enhancement of visual-motor gain in the 96 pursuit system. We argue that the output of FEFSEM dials up visual-motor gain in preparation for 97 a behaviorally-relevant visual motion of a specific direction and speed, and that the use of 98 FEFSEM output as a sensorimotor gain signal allows preparation to proceed without causing 99 movement. We also show that preparatory activity in FEFSEM contradicts the predictions of the 100 dynamical system framework that has arisen from work in arm motor cortex (Churchland et al., 101 2010; Elsayed et al., 2016; Kaufman et al., 2014).102 103 Results 104Here, we present three primary findings to support the conclusion that FEFSEM preparatory 105 activity can evolve without causing smooth pursuit eye movement because its output d...

Drifting population dynamics with transient resets characterize sensorimotor transformation in the monkey superior colliculus

“…Although we consider SC activity during the delay period to be preparatory in the sense that it is related to the enhancement or hindrance of rapid saccade initiation following the go cue, it does not have “motor potential.” In the smooth pursuit system of the FEF, neural activity was found to have motor potential, with partially overlapping subpopulations contributing to both the preparation and execution of movement (Darlington and Lisberger, 2020). However, this does not seem to be the case for the SC, at least in the context of saccades.…”

The effect of temporal expectation on the correlations of frontal neural activity with alpha oscillation and sensory-motor latency

“…Other studies reported an elevated spontaneous activity of FEF neurons toward saccade onset or smooth pursuit onset, which was more pronounced than what we observed here. Those studies typically let the subjects decide when to saccade 32 or anticipate the speed of the upcoming tracking target 40 , 41 . In those cases, spontaneous activity naturally represented the decision processes or prediction of a feature rather than temporal expectations.…”

Sensory-motor computations in a cortico-pontine pathway

“…In the pursuit system, motor preparation modulates the state of visual-motor gain (Kodaka & Kawano, 2003; Tabata et al, 2006). Preparatory enhancement of visual-motor gain has been linked to FEF SEM neurons, which display preparatory ramps of firing during fixation that leads up to pursuit (Darlington & Lisberger, 2020; Mahaffy & Krauzlis, 2011; Tanaka & Fukushima, 1998). Expectation of faster target motion causes larger amplitudes of preparatory activity and larger behavioral readouts of visual-motor gain (Darlington et al, 2018; Darlington et al, 2017).…”

“…Visual-motor gain and FEF SEM have been implicated in many higher-order features of pursuit, for example reward (Raghavan & Joshua, 2017), motor learning (Li & Lisberger, 2011), and modulation of behavior by experience-dependent expectation of target motion (Darlington et al, 2018). Importantly, both visual-motor gain and preparatory activity in FEF SEM are dialed up in preparation for smooth pursuit eye movements (Darlington & Lisberger, 2020; Tabata et al, 2006). It is possible to probe visual-motor gain by measuring the eye movement responses to brief pulses of target motion.…”