Neuronal activity related to visually guided saccadic eye movements in the supplementary motor area of rhesus monkeys

Abstract

1. The purpose of this study was to describe the response properties of neurons in the supplementary motor area (SMA), including the supplementary eye fields (SEF) of three rhesus monkeys (Macaca mulatta) performing visually guided eye and forelimb movements. Seven hundred thirty single units were recorded in the dorsomedial agranular cortex while monkeys performed a go/no-go visual tracking task. The unit activity associated with rewarded, task-related movements was compared with that associated with unrewarded, spontaneous movements executed in the intertrial interval or when the task was not running. A number of neuronal response types were identified. 2. Sensory cells were characterized by their response to the visual and/or auditory target stimuli combined with no discharge associated with eye or forelimb movements. New information was provided about the receptive fields of the visual cells; they varied in size and, although many included the ipsilateral hemifield, they tended to emphasize the contralateral. A significant proportion of the visually responsive cells had receptive fields restricted to within 8 degrees of the fovea. The response latency was relatively long (greater than 90 ms) and variable. 3. Preparatory set cells were activated from the appearance of the target until the presentation of the go/no-go cue. This subpopulation ceased firing 50-100 ms before the movement was initiated. These cells tended to respond best in relation to contralateral movements. The response latency was similar to that of the sensory cells, although some of these units began to discharge in anticipation of predictable target presentations. These neurons were not active before unrewarded, spontaneous saccades. 4. Sensory-movement cells comprised the largest population of neurons identified in SMA. They were active from the appearance of the target until after the execution of the saccade. These neurons tended to respond preferentially in association with contraversive saccades. The latency of response to the target was significantly longer than that of the sensory cells. There was a large amount of variability in the time to reach the peak level of activation, and this population of units generally became inactivated shortly after the saccade was initiated. Although there were counterexamples, most sensory-movement cells responded equally in association with visually and auditory guided movements. In addition, these neurons were not active in relation to self-generated eye movements made during the intertrial intervals. 5. Pause-rebound cells were identified by their suppression at the appearance of the target and subsequent discharge associated with the saccade. These units tended to respond preferentially to contralateral targets.(ABSTRACT TRUNCATED AT 400 WORDS)

Reversible inactivation of macaque dorsomedial frontal cortex: effects on saccades and fixations

“…The nearly omnidirectional deficits conform to prior findings that DMFC visual and presaccadic neurons are tuned for all directions (Schall 1991a) and that contraversive, ipsiversive, and vertical saccades all can be evoked from DMFC (Mann et al 1988;Schall 1991b;Bon and Lucchetti 1992;Tehovnik and Lee 1993;Tehovnik et al 1994;Lee and Tehovnik 1995). A slight contralateral bias in the tuning of DMFC neurons has been reported (Schall 1991a), but we did not observe a corresponding bias in our deficits. We may not have tested enough target locations to uncover such a bias.…”

“…In general, these neurons are poorly tuned for saccade direction (Schall 1991a). Of those that are tuned, a small majority prefer contraversive saccades (Schall 1991a).…”

“…In general, these neurons are poorly tuned for saccade direction (Schall 1991a). Of those that are tuned, a small majority prefer contraversive saccades (Schall 1991a). Other DMFC neurons fire throughout fixation, and many of these begin discharging before or during the saccade that leads to the fixation (Schlag et al 1992;Lee and Tehovnik 1995).…”

“…Many DMFC neurons increase their discharge before or during saccadic eye movements (Brinkman and Porter 1979;Schlag and Schlag-Rey 1987;Mann et al 1988;Schall 1991a;Bon and Lucchetti 1992;Lee and Tehovnik 1995;Russo and Bruce 1996). In general, these neurons are poorly tuned for saccade direction (Schall 1991a).…”

Simultaneous analysis of the LFP and spiking activity reveals essential components of a visuomotor transformation in the frontal eye field

“…The frontal eye field (FEF) is one of the cortical regions that contributes to the visuomotor transformation process by participating in critical events such as target selection (1-3) and saccade preparation (4)(5)(6). In addition to FEF, other oculomotor areas such as the lateral intraparietal cortex (7), the supplementary eye fields (8), the superior colliculus (9), and the dorsolateral prefrontal cortex (10) also possess neurons with similar properties as FEF neurons. Thus, a central question that remains unresolved is to what extent do the response properties of FEF neurons represent a cause versus a consequence of computations occurring elsewhere.…”