An fMRI Investigation of Preparatory Set in the Human Cerebral Cortex and Superior Colliculus for Pro- and Anti-Saccades

Abstract

Previous studies have identified several cortical regions that show larger BOLD responses during preparation and execution of anti-saccades than pro-saccades. We confirmed this finding with a greater BOLD response for anti-saccades than pro-saccades during the preparation phase in the FEF, IPS and DLPFC and in the FEF and IPS in the execution phase. We then applied multi-voxel pattern analysis (MVPA) to establish whether different neural populations are involved in the two types of saccade. Pro-saccades and anti-saccades were reliably decoded during saccade execution in all three cortical regions (FEF, DLPFC and IPS) and in IPS during saccade preparation. This indicates neural specialization, for programming the desired response depending on the task rule, in these regions. In a further study tailored for imaging the superior colliculus in the midbrain a similar magnitude BOLD response was observed for pro-saccades and anti-saccades and the two saccade types could not be decoded with MVPA. This was the case both for activity related to the preparation phase and also for that elicited during the execution phase. We conclude that separate cortical neural populations are involved in the task-specific programming of a saccade while in contrast, the SC has a role in response preparation but may be less involved in high-level, task-specific aspects of the control of saccades.

Socio-cognitive load and social anxiety in an emotional anti-saccade task

“…Using evidence from monkeys, Nguyen et al [ 73 ] have suggested that the superior colliculus begins encoding face like stimuli as early as 25 ms post presentation onset. This may indicate an anticipatory monitoring mechanism which precipitates inhibition as the superior colliculus projects to the oculomotor areas involved with generating pro and anti-saccades and has been linked to the preparation of saccade generation [ 74 ].…”

Mapping neural dynamics underlying saccade preparation and execution and their relation to reaction time and direction errors

“…Conversely, Zhang and Barash (, ) demonstrated that PEF neurons responded to both location and direction, whereby the PEF saccade neurons when aligned to the response field activated 50ms after the visual neurons on the contralateral side of the brain (contralateral to the visual stimulus). Human electrophysiological (Everling, Spantekow, Krappmann, & Flohr, ) and fMRI (Furlan, Smith, & Walker, ) data have demonstrated a switch from contralateral PEF to ipsilateral PEF activity on antisaccade trials demonstrating how PEF is involved in response preparation and motor planning. The FEF is also important for antisaccade generation and is involved in vector inversion: Sato and Schall () found different neurons within the FEF to be involved in visual selection and saccade selection.…”

“…An additional goal in the current study was to identify the time course of activation within the PEF and FEF for prosaccade and antisaccade execution, which are time-aligned to saccade onset. Based on evidence from fMRI (Connolly et al, 2002;DeSouza, Menon, & Everling, 2003;Furlan et al, 2016) and MEG (Herdman & Ryan, 2007) studies, we predicted that prosaccade trials would have more pronounced PEF involvement and antisaccade trials would have more pronounced ipsilateral and contralateral FEF involvement than prosaccade trials.…”

“…Furthermore, it is still unknown how premovement activity within human ipsilateral and contralateral FEF in correct antisaccade trials is related to direction errors. Given the relationship between FEF activity and antisaccade preparation (Connolly et al, ; DeSouza et al, ; Furlan et al, ), we hypothesized that greater neural activity within the contralateral FEF before an antisaccade movement will covary with the proportion of direction errors made in anti‐saccade trials. Concomitantly, a decrease in activity will represent how well a participant can consistently inhibit an automatic saccade, thus making fewer direction errors.…”

Polar-angle representation of saccadic eye movements in human superior colliculus

“…Further, if participants are instructed to make a saccade in the opposite direction of the target, these reverse saccades may resemble an anti-saccade, or an eye-movement away from the cued target. Recent fMRI studies in humans revealed that collicular activity elicited from a saccade towards a target (a pro-saccade) was not distinguishable, via pattern recognition, from anti-saccades (Furlan et al, 2016), suggesting that such anti-saccades could alter topographic measurements. Also, performing anti-saccades may involve the release of inhibitory control exerted by frontal regions like the dorsal lateral prefrontal cortex (DLPFC) onto the colliculus (Condy et al, 2004), which may confound SC topography measurements ( Figure S1).…”