Deficits in Smooth-Pursuit Eye Movements After Muscimol Inactivation Within the Primate's Frontal Eye Field

Abstract

To evaluate smooth-pursuit (SP) function in the primate frontal eye field (FEF), microinjections of muscimol, a gamma-aminobutyric acid (GABA) agonist, were used to reversibly deactivate physiologically characterized sites in FEF. SP was severely impaired by deactivation at sites in the FEF's smooth eye movement region (FEFsem) located in the fundus and posterior bank of the macaque monkey's arcuate sulcus. These SP deficits were apparent immediately after the muscimol injection and persisted for several hours but recovered by the next day. SP was most drastically and consistently impaired for directions similar to the injected site's elicited smooth eye movement direction or to the optimal SP direction for its neuronal responses. Targets moving in these directions, usually ipsilateral to the injected hemisphere, were tracked primarily with saccades after the muscimol injection, the peak SP velocity being only 10-30% of preinjection velocity. SP in other directions, including contralateral, was less strongly affected. Initial SP acceleration in response to target motion onset was also significantly diminished, generally by approximately the same proportion as peak SP velocity. In contrast, saccades were largely unaffected by muscimol injections in FEFsem; nor was there an immediate effect on SP when control sites in the saccadic region of FEF (FEFsac) were deactivated, although a SP deficit often appeared 30-60 min after FEFsac injections, possibly reflecting diffusion of muscimol into neighboring FEFsem. These reversible SP deficits produced by muscimol inactivation within FEFsem are similar to permanent deficits caused by large aspiration lesions of FEF and indicate that inclusion of FEFsem is the critical factor determining whether FEF lesions impair SP. The severity of the reversible deficits found here indicates how extremely critical FEFsem is for normal highgain SP.

Inactivation and stimulation of the frontal pursuit area change pursuit metrics without affecting pursuit target selection

“…Also, the maintained velocity for contraversive pursuit following the inactivation decreased by 1°/s, which was also significantly smaller than the change we observed for ipsiversive pursuit. Thus, consistent with previous studies (e.g., Keating 1991;Lynch 1987;Shi et al 1998), our FPA inactivations produced significant directional defects for late acceleration and steady-state velocity for ipsiversive pursuit.…”

“…In each of our inactivation experiments, we observed significant motor deficits that more strongly affected pursuit ipsiversive to the inactivated side, as expected for unilateral reduction of FPA activity (Lynch 1987;MacAvoy et al 1991;Shi et al 1998). However, we found no evidence of a deficit or bias in the capacity to choose a direction of motion in a pursuit-choice task.…”

“…FPA lesions severely impair pursuit velocity and acceleration and cause permanent impairments in predictive and anticipatory pursuit (Keating 1991(Keating , 1993Keating et al 1996;Lynch 1987;MacAvoy et al 1991); similar deficits in pursuit metrics occur with reversible inactivation (Shi et al 1998). The deficits to pursuit metrics and predictive pursuit are observed for pursuit in all directions but are most strongly expressed for pursuit ipsiversive to the lesion.…”

Neuronal Bases of Directional Expectation and Anticipatory Pursuit

“…Parts of the frontal eye field (FEF) in the fundus and in the posterior bank of the arcuate sulcus are also involved in the control of smooth-pursuit eye movements (Lynch, 1987;Keating, 1991Keating, , 1993MacAvoy et al, 1991;Gottlieb et al, 1993Gottlieb et al, , 1994Tian and Lynch, 1996a,b;Tanaka and Fukushima, 1998;Fukushima et al, 2000;Tanaka and Lisberger, 2001;Carpenter, 2005). Surgical ablation or chemical inactivation of the FEF impairs visually initiated smooth pursuit, suggesting an essential role of this structure in the premotor pathway for pursuit (Lynch, 1987;Keating, 1991;MacAvoy et al, 1991;Shi et al, 1998). One report suggests that the FEF lesion impairs anticipatory and predictive pursuit as well (MacAvoy et al, 1991).…”

Evidence for Object Permanence in the Smooth-Pursuit Eye Movements of Monkeys

“…Despite an imperfect mapping to anatomy, such models can still provide a framework for interpreting (e.g., Shi et al 1998;Tanaka and Lisberger 2001) and suggesting physiological experiments. In the current study, it seems plausible that pursuit engagement is determined by neural activity in the frontal pursuit area.…”