Pursuit Subregion of the Frontal Eye Field Projects to the Caudate Nucleus in Monkeys

2003 ◽  
Vol 89 (5) ◽  
pp. 2678-2684 ◽  
Author(s):  
Dong-Mei Cui ◽  
Yi-Jun Yan ◽  
James C. Lynch
Keyword(s):  
Eye Movements ◽  
Basal Ganglia ◽  
Caudate Nucleus ◽  
Smooth Pursuit ◽  
Saccadic Eye Movements ◽  
Frontal Eye Field ◽  
Smooth Pursuit Eye Movements ◽  
Axon Terminals ◽  
Pursuit Eye Movements ◽  
Eye Field

It has been well established by recording, inactivation, and neuroanatomical studies that the caudate nucleus is important for the control of saccadic eye movements. However, until now, there has been little evidence that the caudate nucleus plays a role in smooth pursuit eye movements. In the present study, we physiologically identified the smooth pursuit subregion of the frontal eye field (FEFsem) and the saccadic subregion of the frontal eye field (FEFsac) in four Cebus monkeys. Anterogradely transported tracers (biotinylated dextran amines and wheat germ aglutinin conjugated to horseradish peroxidase) were then used to determine the efferent connections of the FEFsem to the caudate nucleus and to compare those connections with projections arising in the FEFsac. We observed dense projections from the FEFsem to the head and body of the caudate. The FEFsem and FEFsac terminal fields were of approximately equal density and total area. The region of FEFsem-labeled axon terminals overlapped only slightly with the region of FEFsac-labeled terminals. These results suggest that the caudate nucleus may play an important role in the control of smooth pursuit eye movements via feedback loops involving the basal ganglia and thalamus. Our results further suggest that the basal ganglia circuitry concerned with controlling visual pursuit is physically segregated from that concerned with controlling saccadic eye movements.

scholarly journals Temporal dynamics of retinal and extraretinal signals in the FEFsem during smooth pursuit eye movements

2017 ◽  
Vol 117 (5) ◽  
pp. 1987-2003 ◽  
Author(s):  
Leah Bakst ◽  
Jérome Fleuriet ◽  
Michael J. Mustari
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Clustering Algorithm ◽  
Critical Role ◽  
Image Motion ◽  
Frontal Eye Field ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements ◽  
Eye Field ◽  
Eye Velocity

Neurons in the smooth eye movement subregion of the frontal eye field (FEFsem) are known to play an important role in voluntary smooth pursuit eye movements. Underlying this function are projections to parietal and prefrontal visual association areas and subcortical structures, all known to play vital but differing roles in the execution of smooth pursuit. Additionally, the FEFsem has been shown to carry a diverse array of signals (e.g., eye velocity, acceleration, gain control). We hypothesized that distinct subpopulations of FEFsem neurons subserve these diverse functions and projections, and that the relative weights of retinal and extraretinal signals could form the basis for categorization of units. To investigate this, we used a step-ramp tracking task with a target blink to determine the relative contributions of retinal and extraretinal signals in individual FEFsem neurons throughout pursuit. We found that the contributions of retinal and extraretinal signals to neuronal activity and behavior change throughout the time course of pursuit. A clustering algorithm revealed three distinct neuronal subpopulations: cluster 1 was defined by a higher sensitivity to eye velocity, acceleration, and retinal image motion; cluster 2 had greater activity during blinks; and cluster 3 had significantly greater eye position sensitivity. We also performed a comparison with a sample of medial superior temporal neurons to assess similarities and differences between the two areas. Our results indicate the utility of simple tests such as the target blink for parsing the complex and multifaceted roles of cortical areas in behavior. NEW & NOTEWORTHY The frontal eye field (FEF) is known to play a critical role in volitional smooth pursuit, carrying a variety of signals that are distributed throughout the brain. This study used a novel application of a target blink task during step ramp tracking to determine, in combination with a clustering algorithm, the relative contributions of retinal and extraretinal signals to FEF activity and the extent to which these contributions could form the basis for a categorization of neurons.

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

1998 ◽  
Vol 80 (1) ◽  
pp. 458-464 ◽  
Author(s):  
Dexiu Shi ◽  
Harriet R. Friedman ◽  
Charles J. Bruce
Keyword(s):  
Eye Movements ◽  
Eye Movement ◽  
Smooth Pursuit ◽  
Critical Factor ◽  
Movement Direction ◽  
Frontal Eye Field ◽  
Smooth Pursuit Eye Movements ◽  
Motion Onset ◽  
Pursuit Eye Movements ◽  
Eye Field

Shi, Dexiu, Harriet R. Friedman, and Charles J. Bruce. Deficits in smooth-pursuit eye movements after muscimol inactivation within the primate's frontal eye field. J. Neurophysiol. 80: 458–464, 1998. To evaluate smooth-pursuit (SP) function in the primate frontal eye field (FEF), microinjections of muscimol, a γ-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.

Activity of fixation neurons in the monkey frontal eye field during smooth pursuit eye movements

2014 ◽  
Vol 112 (2) ◽  
pp. 249-262 ◽  
Author(s):  
Yoshiko Izawa ◽  
Hisao Suzuki
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Frontal Eye Field ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements ◽  
Eye Field ◽  
Catch Up ◽  
Discharge Patterns ◽  
Reduced Activity

We recorded the activity of fixation neurons in the frontal eye field (FEF) in trained monkeys and analyzed their activity during smooth pursuit eye movements. Fixation neurons were densely located in the area of the FEF in the caudal part of the arcuate gyrus facing the inferior arcuate sulcus where focal electrical stimulation suppressed the generation of saccades and smooth pursuit in bilateral directions at an intensity lower than the threshold for eliciting electrically evoked saccades. Whereas fixation neurons discharged tonically during fixation, they showed a variety of discharge patterns during smooth pursuit, ranging from a decrease in activity to an increase in activity. Of these, more than two-thirds were found to show a reduction in activity during smooth pursuit in the ipsilateral and bilateral directions. The reduction in activity of fixation neurons began at pursuit initiation and continued during pursuit maintenance. When catch-up saccades during the initiation of pursuit were eliminated by a step-ramp target routine, the reduced activity of fixation neurons remained. The reduction in activity during pursuit was not dependent on the activity during fixation without a target. Based on these results, we discuss the role of the FEF at maintaining fixation in relation to various other brain areas. We suggest that fixation neurons in the FEF contribute to the suppression of smooth pursuit. These results suggest that FEF fixation neurons are part of a more generalized visual fixation system through which suppressive control is exerted on smooth pursuit, as well as saccades.

Smooth-Pursuit Eye-Movement Deficits With Chemical Lesions in Macaque Nucleus Reticularis Tegmenti Pontis

1999 ◽  
Vol 82 (3) ◽  
pp. 1178-1186 ◽  
Author(s):  
David A. Suzuki ◽  
Tetsuto Yamada ◽  
Rebecca Hoedema ◽  
Robert D. Yee
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Ibotenic Acid ◽  
Frontal Eye Field ◽  
Smooth Pursuit Eye Movements ◽  
Pontine Nucleus ◽  
Nucleus Reticularis Tegmenti Pontis ◽  
Pursuit Eye Movements ◽  
Nucleus Reticularis ◽  
Dorsolateral Pontine Nucleus

Anatomic and neuronal recordings suggest that the nucleus reticularis tegmenti pontis (NRTP) of macaques may be a major pontine component of a cortico-ponto-cerebellar pathway that subserves the control of smooth-pursuit eye movements. The existence of such a pathway was implicated by the lack of permanent pursuit impairment after bilateral lesions in the dorsolateral pontine nucleus. To provide more direct evidence that NRTP is involved with regulating smooth-pursuit eye movements, chemical lesions were made in macaque NRTP by injecting either lidocaine or ibotenic acid. Injection sites first were identified by the recording of smooth-pursuit-related modulations in neuronal activity. The resulting lesions caused significant deficits in both the maintenance and the initiation of smooth-pursuit eye movements. After lesion formation, the gain of constant-velocity, maintained smooth-pursuit eye movements decreased, on the average, by 44%. Recovery of the ability to maintain smooth-pursuit eye movements occurred over ∼3 days when maintained pursuit gains attained normal values. The step-ramp, “Rashbass” task was used to investigate the effects of the lesions on the initiation of smooth-pursuit eye movements. Eye accelerations averaged over the initial 80 ms of pursuit initiation were determined and found to be decremented, on the average, by 48% after the administration of ibotenic acid. Impairments in the initiation and maintenance of smooth-pursuit eye movements were directional in nature. Upward pursuit seemed to be the most vulnerable and was impaired in all cases independent of lesioning agent and type of pursuit investigated. Downward smooth pursuit seemed more resistant to the effects of chemical lesions in NRTP. Impairments in horizontal tracking were observed with examples of deficits in ipsilaterally and contralaterally directed pursuit. The results provide behavioral support for the physiologically and anatomic-based conclusion that NRTP is a component of a cortico-ponto-cerebellar circuit that presumably involves the pursuit area of the frontal eye field (FEF) and projects to ocular motor-related areas of the cerebellum. This FEF-NRTP-cerebellum path would parallel a middle and medial superior temporal cerebral cortical area-dorsolateral pontine nucleus-cerebellum pathway also known to be involved with regulating smooth-pursuit eye movements.

Single-neuron activity in the dorsomedial frontal cortex during smooth-pursuit eye movements to predictable target motion

1997 ◽  
Vol 14 (5) ◽  
pp. 853-865 ◽  
Author(s):  
S. J. Heinen ◽  
M. Liu
Keyword(s):  
Eye Movements ◽  
Frontal Cortex ◽  
Smooth Pursuit ◽  
Saccadic Eye Movements ◽  
Target Motion ◽  
Neuron Activity ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements ◽  
Supplementary Eye Field ◽  
Dorsomedial Frontal Cortex

AbstractA region of dorsomedial frontal cortex (DMFC) has been implicated in planning and executing saccadic eye movements; hence it has been referred to as a supplementary eye field (SEF). Recently, activity related to executing smooth-pursuit eye movements has been recorded from the DMFC, and microstimulation here has been shown to evoke smooth eye movements. This report documents neuronal activity present in smooth-pursuit tasks where the predictability of target motion was manipulated. The activity of many neurons in the DMFC reached a peak when a predictable change in target motion occurred. Furthermore, the peak activity of some cells was systematically shifted by manipulating the duration of the target event, indicating that the network these neurons were in could learn the temporal characteristics of new target motion. Finally, the activity of most neurons tested was greater when target motion was predictable than when it was unpredictable. The results suggest that the DMFC participates in planning smooth-pursuit eye movements based on past stimulus history.

Functional Anatomy of Pursuit Eye Movements in Humans as Revealed by fMRI

1999 ◽  
Vol 82 (1) ◽  
pp. 463-471 ◽  
Author(s):  
Laurent Petit ◽  
James V. Haxby
Keyword(s):  
Eye Movements ◽  
Temporal Cortex ◽  
Functional Anatomy ◽  
Saccadic Eye Movements ◽  
Frontal Eye Field ◽  
Pursuit Eye Movements ◽  
Magnetic Imaging ◽  
Supplementary Eye Field ◽  
Eye Field ◽  
Parietal Eye

We have investigated the functional anatomy of pursuit eye movements in humans with functional magnetic imaging. The performance of pursuit eye movements induced activations in the cortical eye fields also activated during the execution of visually guided saccadic eye movements, namely in the precentral cortex [frontal eye field (FEF)], the medial superior frontal cortex (supplementary eye field), the intraparietal cortex (parietal eye field), and the precuneus, and at the junction of occipital and temporal cortex (MT/MST) cortex. Pursuit-related areas could be distinguished from saccade-related areas both in terms of spatial extent and location. Pursuit-related areas were smaller than their saccade-related counterparts, three of eight significantly so. The pursuit-related FEF was usually inferior to saccade-related FEF. Other pursuit-related areas were consistently posterior to their saccade-related counterparts. The current findings provide the first functional imaging evidence for a distinction between two parallel cortical systems that subserve pursuit and saccadic eye movements in humans.

Extraretinal Inputs to Neurons in the Rostral Superior Colliculus of the Monkey During Smooth-Pursuit Eye Movements

2001 ◽  
Vol 86 (5) ◽  
pp. 2629-2633 ◽  
Author(s):  
Richard J. Krauzlis
Keyword(s):  
Eye Movements ◽  
Superior Colliculus ◽  
Smooth Pursuit ◽  
Saccadic Eye Movements ◽  
Visual Response ◽  
Smooth Pursuit Eye Movements ◽  
Related Activity ◽  
Pursuit Eye Movements ◽  
Deep Layers ◽  
Almost All

The intermediate and deep layers of the monkey superior colliculus (SC) are known to be important for the generation of saccadic eye movements. Recent studies have also provided evidence that the rostral SC might be involved in the control of pursuit eye movements. However, because rostral SC neurons respond to visual stimuli used to guide pursuit, it is also possible that the pursuit-related activity is simply a visual response. To test this possibility, we recorded the activity of neurons in the rostral SC as monkeys smoothly pursued a target that was briefly extinguished. We found that almost all rostral SC neurons in our sample maintained their pursuit-related activity during a brief visual blink, which was similar to the maintained activity they also exhibited during blinks imposed during fixation. These results indicate that discharge of rostral SC neurons during pursuit is not simply a visual response, but includes extraretinal signals.

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