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 Role of Arcuate Frontal Cortex of Monkeys in Smooth Pursuit Eye Movements. I. Basic Response Properties to Retinal Image Motion and Position

2002 ◽  
Vol 87 (6) ◽  
pp. 2684-2699 ◽  
Author(s):  
Masaki Tanaka ◽  
Stephen G. Lisberger
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Retinal Image ◽  
Image Motion ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements ◽  
Wide Range ◽  
Image Position ◽  
Eye Velocity ◽  
Pursuit Neurons

Anatomical and physiological studies have shown that the “frontal pursuit area” (FPA) in the arcuate cortex of monkeys is involved in the control of smooth pursuit eye movements. To further analyze the signals carried by the FPA, we examined the activity of pursuit-related neurons recorded from a discrete region near the arcuate spur during a variety of oculomotor tasks. Pursuit neurons showed direction tuning with a wide range of preferred directions and a mean full width at half-maximum of 129°. Analysis of latency using the “receiver operating characteristic” to compare responses to target motion in opposite directions showed that the directional response of 58% of FPA neurons led the initiation of pursuit, while 19% led by 25 ms or more. Analysis of neuronal responses during pursuit of a range of target velocities revealed that the sensitivity to eye velocity was larger during the initiation of pursuit than during the maintenance of pursuit, consistent with two components of firing related to image motion and eye motion. FPA neurons showed correlates of two behavioral features of pursuit documented in prior reports. 1) Eye acceleration at the initiation of pursuit declines as a function of the eccentricity of the moving target. FPA neurons show decreased firing at the initiation of pursuit in parallel with the decline in eye acceleration. This finding is consistent with prior suggestions that the FPA plays a role in modulating the gain of visual-motor transmission for pursuit. 2) A stationary eccentric cue evokes a smooth eye movement opposite in direction to the cue and enhances the pursuit evoked by subsequent target motions. Many pursuit neurons in the FPA showed weak, phasic visual responses for stationary targets and were tuned for the positions about 4° eccentric on the side opposite to the preferred pursuit direction. However, few neurons (12%) responded during the preparation or execution of saccades. The responses to the stationary target could account for the behavioral effects of stationary, eccentric cues. Further analysis of the relationship between firing rate and retinal position error during pursuit in the preferred and opposite directions failed to provide evidence for a large contribution of image position to the firing of FPA neurons. We conclude that FPA processes information in terms of image and eye velocity and that it is functionally separate from the saccadic frontal eye fields, which processes information in terms of retinal image position.

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.

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.

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.

Neuronal Responses Related to Smooth Pursuit Eye Movements in the Periarcuate Cortical Area of Monkeys

1998 ◽  
Vol 80 (1) ◽  
pp. 28-47 ◽  
Author(s):  
Masaki Tanaka ◽  
Kikuro Fukushima
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Cortical Area ◽  
Eye Position ◽  
Smooth Pursuit Eye Movements ◽  
Neuronal Responses ◽  
Stationary Target ◽  
Pursuit Eye Movements ◽  
Preferred Direction ◽  
Eye Velocity

Tanaka, Masaki and Kikuro Fukushima. Neuronal responses related to smooth pursuit eye movements in the periarcuate cortical area of monkeys. J. Neurophysiol. 80: 28–47, 1998. To examine how the periarcuate area is involved in the control of smooth pursuit eye movements, we recorded 177 single neurons while monkeys pursued a moving target in the dark. The majority (52%, 92/177) of task-related neurons responded to pursuit but had little or no response to saccades. Histological reconstructions showed that these neurons were located mainly in the posterior bank of the arcuate sulcus near the sulcal spur. Twenty-seven percent (48/177) changed their activity at the onset of saccades. Of these, 36 (75%) showed presaccadic burst activity with strong preference for contraversive saccades. Eighteen (10%, 18/177) were classified as eye-position–related neurons, and 11% (19/177) were related to other aspects of the stimuli or response. Among the 92 neurons that responded to pursuit, 85 (92%) were strongly directional with uniformly distributed preferred directions. Further analyses were performed in these directionally sensitive pursuit-related neurons. For 59 neurons that showed distinct changes in activity around the initiation of pursuit, the median latency from target motion was 96 ms and that preceding pursuit was −12 ms, indicating that these neuron can influence the initiation of pursuit. We tested some neurons by briefly extinguishing the tracking target ( n = 39) or controlling its movement with the eye position signal ( n = 24). The distribution of the change in pursuit-related activity was similar to previous data for the dorsomedial part of the medial superior temporal neurons ( Newsome et al. 1988) , indicating that pursuit-related neurons in the periarcuate area also carry extraretinal signals. For 22 neurons, we examined the responses when the animals reversed pursuit direction to distinguish the effects of eye acceleration in the preferred direction from oppositely directed eye velocity. Almost all neurons discharged before eye velocity reached zero, however, only nine neurons discharged before the eyes were accelerated in the preferred direction. The delay in neuronal responses relative to the onset of eye acceleration in these trials might be caused by suppression from oppositely directed pursuit velocity. The results suggest that the periarcuate neurons do not participate in the earliest stage of eye acceleration during the change in pursuit direction, although most of them may participate in the early stages of pursuit initiation in the ordinary step-ramp pursuit trials. Some neurons changed their activity when the animals fixated a stationary target, and this activity could be distinguished easily from the strong pursuit-related responses. Our results suggest that the periarcuate pursuit area carries extraretinal signals and affects the premotor circuitry for smooth pursuit.

scholarly journals Illusory bending of a rigidly moving line segment: Effects of image motion and smooth pursuit eye movements

10.1167/7.6.9 ◽  
2007 ◽  
Vol 7 (6) ◽  
pp. 9 ◽  
Author(s):  
Lore Thaler ◽  
James T. Todd ◽  
Miriam Spering ◽  
Karl R. Gegenfurtner
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Line Segment ◽  
Image Motion ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements ◽  
Moving Line
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