Distinct Neural Correlates for Volitional Generation and Inhibition of Saccades

Abstract

The antisaccade task has proven highly useful in basic and clinical neuroscience, and the neural structures involved are well documented. However, the cognitive and neural mechanisms that mediate task performance are not yet understood. An event-related fMRI study was designed to dissociate the neural correlates of two putative key functions, volitional saccade generation and inhibition of reflexive saccades, and to investigate their interaction. Nineteen healthy volunteers performed a task that required (a) to initiate saccades volitionally, either with or without a simultaneous demand to inhibit a reflexive saccade; and (b) to inhibit a reflexive saccade, either with or without a simultaneous demand to initiate a saccade volitionally. Analysis of blood oxygen level-dependent signal changes confirmed a major role of the frontal eye fields and the supplementary eye fields in volitional saccade generation. Inhibition-related activation of a specific fronto-parietal network was highly consistent with previous evidence involved in inhibitory processes. Unexpectedly, there was little evidence of specific brain activation during combined generation and inhibition demands, suggesting that the neural processing of generation and inhibition in antisaccades is independent to a large extent.

Dissociating Bottom-Up and Top-Down Processes in a Manual Stimulus–Response Compatibility Task

“…This interpretation is well in line with a study trying to separate the volitional generation component from inhibitory processes in the antisaccade task (Reuter et al 2010). These authors found the FEFs and supplementary eye field (SEF) to be specifically involved in the preparation component of volitional saccades generation, suggesting that the neural components for generation and inhibition of saccades are independent to a large extent.…”

“…This process then leads to a facilitation of the congruent response (Eimer et al 1995;Rubichi et al 1997;Sheliga et al 1997). In contrast, incongruent responses require an indirect task-dependent response selection process including inhibition of the automatic response facilitated by the reflexive reorientation, endogenous reorienting of attentional properties to the opposite side, and volitional response initiation (Munoz and Everling 2004;Nee et al 2007;Reuter et al 2010).…”

“…Several lines of evidence for differential involvement of the frontoparietal network for stimulus-driven and context-dependent eye movements have been investigated in great detail with human neuroimaging studies as well as electrophysiological recordings in monkeys using the pro-/antisaccade task (e.g., Munoz and Everling 2004;Reuter et al 2010). In contrast, imaging studies investigating the functional anatomy of the compatibility effect for hand movements have mostly focused on the effect of interference resolution during incongruent responses.…”

Antisaccade performance in schizophrenia patients, their first-degree biological relatives, and community comparison subjects: Data from the COGS study

“…One way of assessing inhibitory processes is through carefully designed cognitive tasks such as the antisaccade task, which was first described by Hallett (1978). Although a number of cognitive processes may be important for the correct execution of an antisaccade (Hutton, 2008; McDowell, Dyckman, Austin,& Clementz, 2008), there is compelling evidence that inhibitory processes are active during the performance of antisaccade tasks (Nyffeler, Müri, Bucher-Ottiger, Pierrot-Deseilligny, Gaymard, & Rivaud-Pechoux, 2007; Reuter, Kaufmann, Bender, Pinkpank, & Kathmann, 2010). Behaviorally, the antisaccade task relies on the fact that, when presented with a visual stimulus, higher primates will reflexively make a saccade to focus on the stimulus.…”

Facing competition: Neural mechanisms underlying parallel programming of antisaccades and prosaccades

“…Stronger activations in the prefrontal cortex (IFG, MFG, SFG) may reflect the highly volitional nature of prosaccades in the present paradigm, as mentioned above. These additional frontal activations may serve a supervisory role in saccade generation (Brown et al, 2006;Ford et al, 2005;Reuter, Kaufmann, Bender, Pinkpank, & Kathmann, 2010) and attenuate the otherwise automatic nature of prosaccades to ensure correct saccade performance.…”