Attentional control of smooth pursuit eye movements: insights from Parkinson’s and Huntington’s diseases

A topical issue in current ocular motor research is the extent to which saccadic and smooth pursuit (SP) eye movements are influenced by the same attentional mechanisms. The basal ganglia (BG) form a critical node within saccade and SP circuitry, and are strongly implicated in resolving conflict between competing response alternatives, a key component of attentional control. Albeit a simplistic account, the BG are thought to achieve this by modulating the balance of facilitatory and inhibitory activity relayed to interconnecting areas. Parkinson’s disease (PD) and Huntington’s disease (HD) are neurodegenerative disorders, which are primarily associated with preferential degradation of BG pathways early in the disease process. Over a range of behavioural tasks, including saccades, PD and HD patients exhibit reliably distinct deficit profiles that correspond with specific sites of BG dysfunction. Individuals with PD typically demonstrate significant difficulty initiating and facilitating desired behaviour as well as gating competing responses. This is thought to reflect enhanced BG inhibitory output. Conversely, HD is associated with difficulty suppressing neural activity and perseverative behaviour, consistent with reduced BG inhibitory modulation. To further explore the functional overlap between saccades and SP, and to more fully characterise the behavioural deficits associated with PD and HD, the present thesis explored a range of attentional phenomena in the context of SP eye movements. In keeping with the role of the BG in conflict resolution, all tasks were designed to elicit competing facilitatory and inhibitory processes. The first experimental study explored the ability to inhibit a prepotent, automatic response to a distractor stimulus while actively tracking a moving target. While PD patients experienced considerable difficulty gating inappropriate responses to distractor stimuli, HD patients were able to withhold an erroneous response, contrary to previous reports of distractibility in HD. The second experiment evaluated control of automatic attentional processes using an exogenous cueing task. Unlike the PD group, the HD group were proficient at suppressing erroneous responses to the salient cue. Further, while HD patients showed no response facilitation following valid cues, PD patients exhibited comparable cueing effects to controls. There was no evidence of inhibition of return for any group. The final experiment examined the influence of goal-directed attention on SP behaviour using a directionally informative endogenous cue. This task revealed a similar group dissociation in the ability to withhold an erroneous response corresponding with cue directives. PD patients exhibited significant difficulty facilitating SP over time, while HD patients demonstrated reduced response facilitation following valid cues. The observed profile of deficits is compatible with the respective sites of BG dysfunction associated with PD and HD. Compromised BG function affects not only basic motor activity, but also the higher order cognitive mechanisms that underlie behavioural control more generally. Collectively, these results were broadly consistent with the range of difficulties previously reported in saccades and general motor control in PD and HD, with differences likely attributable to disparities in the decision thresholds for executing a response between the various movement types. Thus, using a disease model, the current investigation has advanced our understanding of the SP system and how it relates to the saccadic system, as well as furthering our conceptual understanding of how the brain controls movement more generally