Frontal Eye Field Inactivation Reduces Saccade Preparation in the Superior Colliculus but Does Not Alter How Preparatory Activity Relates to Saccades of a Given Latency

Abstract

A neural correlate for saccadic reaction times (SRTs) in the gap saccade task is the level of low-frequency activity in the intermediate layers of the superior colliculus (iSC) just before visual target onset: greater levels of such preparatory iSC low-frequency activity precede shorter SRTs. The frontal eye fields (FEFs) are one likely source of iSC preparatory activity, since FEF preparatory activity is also inversely related to SRT. To better understand the FEF’s role in saccade preparation, and the way in which such preparation relates to SRT, in two male rhesus monkeys, we compared iSC preparatory activity across unilateral reversible cryogenic inactivation of the FEF. FEF inactivation increased contralesional SRTs, and lowered ipsilesional iSC preparatory activity. FEF inactivation also reduced rostral iSC activity during the gap period. Importantly, the distributions of SRTs generated with or without FEF inactivation overlapped, enabling us to conduct a novel population-level analyses examining iSC preparatory activity just before generation of SRT-matched saccades. When matched for SRTs, we observed no change during FEF inactivation in the relationship between iSC preparatory activity and SRT-matched saccades across a range of SRTs, even for the occasional express saccade. Thus, while our results emphasize that the FEF has an overall excitatory influence on preparatory activity in the iSC, the communication between the iSC and downstream oculomotor brainstem is unaltered for SRT-matched saccades.

Role of the frontal eye field in human pupil and saccade orienting responses

“…This coordination between pupil size and saccades is also observed in human studies in the tasks involving pro‐ or anti‐saccade generation (Dalmaso et al., 2020; Jainta et al., 2011; Wang et al., 2015, 2016, 2017). Trials with faster SRTs accompany trials with larger pupil dilation responses, arguably through low‐frequency saccade preparatory activity observed in the FEF and SC (Basso & Wurtz, 1998; Dash et al., 2018; Dorris et al., 1997; Everling & Munoz, 2000; Jagadisan & Gandhi, 2017; Krauzlis, 2003). Furthermore, a recent monkey study has showed decreased SC preparatory activity after FEF inactivation (Dash et al., 2018).…”

“…Trials with faster SRTs accompany trials with larger pupil dilation responses, arguably through low‐frequency saccade preparatory activity observed in the FEF and SC (Basso & Wurtz, 1998; Dash et al., 2018; Dorris et al., 1997; Everling & Munoz, 2000; Jagadisan & Gandhi, 2017; Krauzlis, 2003). Furthermore, a recent monkey study has showed decreased SC preparatory activity after FEF inactivation (Dash et al., 2018). Consistently, here we found correlations between pupil size and SRTs in the contralateral condition in the vertex stimulation, and the diminished correlation with FEF stimulation, suggesting a role of human FEF in mediating this coupling between pupil size and SRTs.…”

“…The frontal eye field (FEF) closely connects to the SC anatomically and physiologically (Everling & Munoz, 2000; Komatsu & Suzuki, 1985; Schlag‐Rey et al., 1992; Segraves & Goldberg, 1987; Sommer & Wurtz, 2000; Stanton et al., 1988). The FEF, together with the SC, is causally involved in saccade generation, as electrical microstimulation of either area elicits saccades, and inactivation of either area causes deficits for saccades made to the visual field coordinated by the affected areas (Aizawa & Wurtz, 1998; Bruce et al., 1985; Dash et al., 2018, 2020; Dias et al., 1995; Dias & Segraves, 1999; Hikosaka & Wurtz, 1985, 1986; Lee et al., 1988; Peel et al., 2014, 2017; Robinson, 1972; Robinson & Fuchs, 1969; Schiller & Stryker, 1972; Sommer & Tehovnik, 1997).…”

Trial-by-trial modulation of express visuomotor responses induced by symbolic or barely detectable cues

“…Peel et al (2017) reported activity decrements of the superior colliculus neurons when the frontal-eye-field in monkeys was cryogenically inactivated. More recently, Dash et al (2018) showed that FEF inactivation correlated with reduced occurrence of express saccades relative to control conditions. Critically, these findings indicate that the cortical top-down signals to the superior colliculus can modulate the express visuomotor transformations operated by this midbrain structure.…”

Dissociable Roles of FEF Neurons in Initiating Saccades

“…A causal role of the frontal eye field (FEF) in initiating and overall in generating saccades has been demonstrated in two ways: Electrical microstimulation of this region evokes saccades (Bruce et al, 1985; Opris et al, 2001; Robinson and Fuchs, 1969) and its pharmacological inactivation impairs the generation of saccades (Dash et al, 2018; Sommer and Tehovnik, 1997). To explain how single neurons in this region could contribute to saccade initiation, (Hanes and Schall, 1996) suggested a “variable rate” model.…”