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

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.

2000 ◽  
Vol 84 (2) ◽  
pp. 892-908 ◽  
Author(s):  
Michele A. Basso ◽  
Richard J. Krauzlis ◽  
Robert H. Wurtz

Neurons in the intermediate and deep layers of the rostral superior colliculus (SC) of monkeys are active during attentive fixation, small saccades, and smooth-pursuit eye movements. Alterations of SC activity have been shown to alter saccades and fixation, but similar manipulations have not been shown to influence smooth-pursuit eye movements. Therefore we both activated (electrical stimulation) and inactivated (reversible chemical injection) rostral SC neurons to establish a causal role for the activity of these neurons in smooth pursuit. First, we stimulated the rostral SC during pursuit initiation as well as pursuit maintenance. For pursuit initiation, stimulation of the rostral SC suppressed pursuit to ipsiversive moving targets primarily and had modest effects on contraversive pursuit. The effect of stimulation on pursuit varied with the location of the stimulation with the most rostral sites producing the most effective inhibition of ipsiversive pursuit. Stimulation was more effective on higher pursuit speeds than on lower and did not evoke smooth-pursuit eye movements during fixation. As with the effects on pursuit initiation, ipsiversive maintained pursuit was suppressed, whereas contraversive pursuit was less affected. The stimulation effect on smooth pursuit did not result from a generalized inhibition because the suppression of smooth pursuit was greater than the suppression of smooth eye movements evoked by head rotations (vestibular-ocular reflex). Nor was the stimulation effect due to the activation of superficial layer visual neurons rather than the intermediate layers of the SC because stimulation of the superficial layers produced effects opposite to those found with intermediate layer stimulation. Second, we inactivated the rostral SC with muscimol and found that contraversive pursuit initiation was reduced and ipsiversive pursuit was increased slightly, changes that were opposite to those resulting from stimulation. The results of both the stimulation and the muscimol injection experiments on pursuit are consistent with the effects of these activation and inactivation experiments on saccades, and the effects on pursuit are consistent with the hypothesis that the SC provides a position signal that is used by the smooth-pursuit eye-movement system.


2000 ◽  
Vol 84 (2) ◽  
pp. 876-891 ◽  
Author(s):  
Richard J. Krauzlis ◽  
Michele A. Basso ◽  
Robert H. Wurtz

The intermediate and deep layers of the monkey superior colliculus (SC) comprise a retinotopically organized map for eye movements. The rostral end of this map, corresponding to the representation of the fovea, contains neurons that have been referred to as “fixation cells” because they discharge tonically during active fixation and pause during the generation of most saccades. These neurons also possess movement fields and are most active for targets close to the fixation point. Because the parafoveal locations encoded by these neurons are also important for guiding pursuit eye movements, we studied these neurons in two monkeys as they generated smooth pursuit. We found that fixation cells exhibit the same directional preferences during pursuit as during small saccades—they increase their discharge during movements toward the contralateral side and decrease their discharge during movements toward the ipsilateral side. This pursuit-related activity could be observed during saccade-free pursuit and was not predictive of small saccades that often accompanied pursuit. When we plotted the discharge rate from individual neurons during pursuit as a function of the position error associated with the moving target, we found tuning curves with peaks within a few degrees contralateral of the fovea. We compared these pursuit-related tuning curves from each neuron to the tuning curves for a saccade task from which we separately measured the visual, delay, and peri-saccadic activity. We found the highest and most consistent correlation with the delay activity recorded while the monkey viewed parafoveal stimuli during fixation. The directional preferences exhibited during pursuit can therefore be attributed to the tuning of these neurons for contralateral locations near the fovea. These results support the idea that fixation cells are the rostral extension of the buildup neurons found in the more caudal colliculus and that their activity conveys information about the size of the mismatch between a parafoveal stimulus and the currently foveated location. Because the generation of pursuit requires a break from fixation, the pursuit-related activity indicates that these neurons are not strictly involved with maintaining fixation. Conversely, because activity during the delay period was found for many neurons even when no eye movement was made, these neurons are also not obligatorily related to the generation of a movement. Thus the tonic activity of these rostral neurons provides a potential position-error signal rather than a motor command—a principle that may be applicable to buildup neurons elsewhere in the SC.


1997 ◽  
Vol 14 (5) ◽  
pp. 853-865 ◽  
Author(s):  
S. J. Heinen ◽  
M. Liu

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.


2003 ◽  
Vol 89 (5) ◽  
pp. 2678-2684 ◽  
Author(s):  
Dong-Mei Cui ◽  
Yi-Jun Yan ◽  
James C. Lynch

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.


2011 ◽  
Vol 70 ◽  
pp. 352-352 ◽  
Author(s):  
K Strand Brodd ◽  
K Rosander ◽  
H Grönqvist ◽  
G Holmström ◽  
B Strömberg ◽  
...  

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