Actions are guided by a Bayesian-like interaction between priors based on experience and current sensory evidence. Here we unveil a complete neural implementation of Bayesian-like behavior, including adaptation of a prior. We recorded the spiking of single neurons in the smooth eye-movement region of the frontal eye fields (FEF), a region that is causally involved in smooth-pursuit eye movements. Monkeys tracked moving targets in contexts that set different priors for target speed. Before the onset of target motion, preparatory activity encodes and adapts in parallel with the behavioral adaptation of the prior. During the initiation of pursuit, FEF output encodes a maximum a posteriori estimate of target speed based on a reliability-weighted combination of the prior and sensory evidence. FEF responses during pursuit are sufficient both to adapt a prior that may be stored in FEF and, through known downstream pathways, to cause Bayesian-like behavior in pursuit.

Bayesian inference provides a cogent account of how the brain combines sensory information with "priors" based on past experience to guide many behaviors, including smooth pursuit eye movements. We now demonstrate very rapid adaptation of the pursuit system's priors for target direction and speed. We go on to leverage that adaptation to outline possible neural mechanisms that could cause pursuit to show features consistent with Bayesian inference. Adaptation of the prior causes changes in the eye speed and direction at the initiation of pursuit. The adaptation appears after a single trial and accumulates over repeated exposure to a given history of target speeds and directions. The influence of the priors depends on the reliability of visual motion signals: priors are more effective against the visual motion signals provided by low-contrast vs. high-contrast targets. Adaptation of the direction prior generalizes to eye speed and vice versa, suggesting that both priors could be controlled by a single neural mechanism. We conclude that the pursuit system can learn the statistics of visual motion rapidly and use those statistics to guide future behavior. Furthermore, a model that adjusts the gain of visual-motor transmission predicts the effects of recent experience on pursuit direction and speed, as well as the specifics of the generalization between the priors for speed and direction. We suggest that Bayesian inference in pursuit behavior is implemented by distinctly non-Bayesian internal mechanisms that use the smooth eye movement region of the frontal eye fields to control of the gain of visual-motor transmission. Bayesian inference can account for the interaction between sensory data and past experience in many behaviors. Here, we show, using smooth pursuit eye movements, that the priors based on past experience can be adapted over a very short time frame. We also show that a single model based on direction-specific adaptation of the strength of visual-motor transmission can explain the implementation and adaptation of priors for both target direction and target speed.

We seek a neural circuit explanation for sensory-motor reaction times. In the smooth eye movement region of the frontal eye fields (FEFSEM), the latencies of pairs of neurons show trial-by-trial correlations that cause trial-by-trial correlations in neural and behavioral latency. These correlations can account for two-third of the observed variation in behavioral latency. The amplitude of preparatory activity also could contribute, but the responses of many FEFSEM neurons fail to support predictions of the traditional “ramp-to-threshold” model. As a correlate of neural processing that determines reaction time, the local field potential in FEFSEM includes a brief wave in the 5–15-Hz frequency range that precedes pursuit initiation and whose phase is correlated with the latency of pursuit in individual trials. We suggest that the latency of the incoming visual motion signals combines with the state of preparatory activity to determine the latency of the transient response that controls eye movement. Impact statement The motor cortex for smooth pursuit eye movements contributes to sensory-motor reaction time through the amplitude of preparatory activity and the latency of transient, visually driven responses.

We reveal a novel mechanism that explains how preparatory activity can evolve in motor-related cortical areas without prematurely inducing movement. The smooth eye movement region of the frontal eye fields (FEFSEM) is a critical node in the neural circuit controlling smooth pursuit eye movement. Preparatory activity evolves in the monkey FEFSEM during fixation in parallel with an objective measure of visual-motor gain. We propose that the use of FEFSEM output as a gain signal rather than a movement command allows for preparation to progress in pursuit without causing movement. We also show that preparatory modulation of firing rate in FEFSEM predicts movement, providing evidence against the ‘movement-null’ space hypothesis as an explanation of how preparatory activity can progress without movement. Finally, there is a partial reorganization of FEFSEM population activity between preparation and movement that would allow for a directionally non-specific component of preparatory visual-motor gain enhancement in pursuit.

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...