Controlled Movement Processing: Superior Colliculus Activity Associated with Countermanded Saccades

Abstract

We investigated whether the monkey superior colliculus (SC), an important midbrain structure for the regulation of saccadic eye movements, contains neurons with activity patterns sufficient to control both the cancellation and the production of saccades. We used a countermanding task to manipulate the probability that, after the presentation of a stop signal, the monkeys canceled a saccade that was planned in response to an eccentric visual stimulus. By modeling each animal's behavioral responses, with a race between GO and STOP processes leading up to either saccade initiation or cancellation, we estimated that saccade cancellation took on average 110 msec. Neurons recorded in the superior colliculus intermediate layers during this task exhibited the discharge properties expected from neurons closely involved in behavioral control. Both saccade- and fixation-related discharged differently when saccades were counter-manded instead of executed, and the time at which they changed their activity preceded the behavioral estimate of saccade cancellation obtained from the same trials by 10 and 13 msec, respectively. Furthermore, these intervals exceed the minimal amount of time needed for SC activity to influence eye movements. The additional observation that saccade-related neurons discharged significantly less when saccades were countermanded instead of executed suggests that saccades are triggered when these neurons reach a critical activation level. Altogether, these findings provide solid evidence that the superior colliculus contains the necessary neural signals to be directly involved in the decision process that regulates whether a saccade is to be produced.

A Within Trial Measure of the Stop Signal Reaction Time in a Head-Unrestrained Oculomotor Countermanding Task

“…Second, if antagonist neck muscle activity arises from response conflict, then such neck muscle activity should appear on every STOP trial. Neurophysiological correlates of the GO and STOP process are present on every STOP trial regardless of outcome (Hanes et al 1998;Paré and Hanes 2003). Instead our data clearly show that antagonist neck muscle activity arises only on a subset of STOP trials (Fig.…”

“…Recordings in the FEF and SC of head-restrained monkeys have determined that the timing of the silencing of movement-related neurons and the simultaneous re-activation of fixation-related neurons is appropriate to mediate the control of saccades (Hanes et al 1998;Paré and Hanes 2003). However, it is unlikely that either of these mechanisms could directly recruit the antagonist muscle activity observed on head-only errors.…”

“…Estimation of the SSRT provides a metric for movement cancellation that has been used, for example, to quantify control deficits following brain damage (Dimitrov et al 2003) and the effects of pharmaceuticals on children with attention deficit hyperactivity disorder (Tannock et al 1995; see Verbruggen and Logan 2008 for review). SSRT estimates are also useful neurophysiologically in assessing whether a given area is involved in the immediate control of action or not (Hanes et al 1998;Paré and Hanes 2003;Stuphorn et al 2000).…”

On the Dissociation between Microsaccade Rate and Direction after Peripheral Cues: Microsaccadic Inhibition Revisited

“…Our hypothesis is that such resetting occurs through a countermanding process that cancels an upcoming microsaccade and initiates a competing one. Evidence for the operation of such a process in the SC exists for large saccades (Paré and Hanes, 2003), making it likely that it also operates for microsaccades.…”

“…Thus, the inhibition need not be the result of a reduction of foveal SC activity. An additional possibility is that inhibition reflects an increased effective threshold for triggering microsaccades (which could be achieved by altering the M buildup rate, as observed in the SC for large saccades) (Paré and Hanes, 2003). For example, Hafed et al (2009) proposed that a microsaccade would be triggered if the instantaneous center of mass of SC activity deviates away from straight ahead by a certain predetermined threshold.…”