Role of the human supplementary eye field in the control of saccadic eye movements

Abstract

The precise function of the supplementary eye field (SEF) is poorly understood. Although electrophysiological and functional imaging studies are important for demonstrating when SEF neurones are active, lesion studies are critical to establish the functions for which the SEF is essential. Here we report a series of investigations performed on an extremely rare individual with a highly focal lesion of the medial frontal cortex. High-resolution structural imaging demonstrated that his lesion was confined to the region of the left paracentral sulcus, the anatomical locus of the SEF. Behavioural testing revealed that the patient was significantly impaired when required to switch between anti- and pro-saccades, when there were conflicting rules governing stimulus–response mappings for saccades. Similarly, the results of an arbitrary stimulus–response associative learning task demonstrated that he was impaired when required to select the appropriate saccade from conflicting eye movement responses, but not for limb movements on an analogous manual task. When making memory-guided saccadic sequences, the patient demonstrated hypometria, like patients with Parkinson's disease, but had no significant difficulties in reproducing the order of saccades correctly on a task that emphasized accuracy with a wide temporal segregation between responses. These findings are consistent with the hypothesis that the SEF plays a key role in implementing control when there is conflict between several, ongoing competing saccadic responses, but not when eye movements need to be made accurately in sequence.

Executive control of gaze by the frontal lobes

“…In addition, these neurons in the SEF modulated after the stop signal reaction time on canceled trials, which is too late to exert any control over saccade initiation. These observations are consistent with observations that lesions of the SEF cause only a relatively modest impairment of gaze (Schiller & Chou, 2000; see also Husain, Parton, Hodgson, Mort, & Rees, 2003;Parton et al, 2007). On the other hand, following combined ablation of the FEF and the SC, leaving the SEF intact, monkeys cannot produce saccadic eye movements (Schiller, True, & Conway, 1980).…”

“…Although interpreting signals in the ACC in terms of monitoring performance is not novel, this interpretation of the SEF is a new perspective. However, this framework has been supported by new evidence from functional brain imaging studies (Curtis, Cole, Rao, & D'Esposito, 2005;Nachev, Rees, Parton, Kennard, & Husain, 2005) and effects of localized lesions (e.g., Parton et al, 2007;Sumner et al, 2007).…”

“…Activity in the SEF is elevated for antisaccades, relative to prosaccades (Amador, Schlag-Rey, & Schlag, 2004), whereas activity in the FEF and SC is reduced (Everling & Munoz, 2000;Everling, Dorris, Klein, & Munoz, 1999; but see Sato & Schall, 2003). Also, damage to the human SEF resulted in self-monitoring deficits (Husain et al, 2003;Parton et al, 2007), and an f MRI signal occurs in the SEF when subjects change plans during conflict (Nachev et al, 2005).…”

Rank Signals in Four Areas of Macaque Frontal Cortex During Selection of Actions and Objects in Serial Order

“…Early clinical studies of human patients with the SEF lesions reported moderately poor performance in tasks requiring two or more memory guided saccades (Gaymard et al 1998;Pierrot-Deseilligny et al 1995). However, a more recent study of a patient with a rare highly focal lesion of the SEF reported no significant deficit with respect to the order of a sequence of memoryguided saccades (Parton et al 2007). …”

Cognition and Eye Movements

“…The ocular motor networks substantially overlie the hemispheric attentional systems in frontal, temporal, and parietal lobes (7), interacting at many levels (8)(9)(10)(11)(12)(13)(14)(15)(16)(17). Cognitive processes are most readily examined with saccades.…”