Minimal synaptic delay in the saccadic output pathway of the superior colliculus studied in awake monkey

Miyashita, Nobuo; Hikosaka, Okihide

doi:10.1007/bf00227637

Cited by 59 publications

(57 citation statements)

References 43 publications

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“…Figure 4a plots mean head latency as a function of mean gaze latency for the 21 stimulation sites tested with the head free to move. The mean ± SD gaze latency was 14.3 ± 7.9 ms (median: 13.3 ms; range: 3.6-37.7 ms) (Note that the 3.6 ms is less than the 4.8 ± 0.5 ms reported for midflight electrical stimulation of the PPRF (Miyashita and Hikosaka 1996). This difference is attributed to our low velocity threshold criterion and/or the visual inspection method in the previous study).…”

Section: Eye-head Coordinationmentioning

confidence: 61%

Coordination of eye and head components of movements evoked by stimulation of the paramedian pontine reticular formation

2008

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Constant frequency microstimulation of the paramedian pontine reticular formation (PPRF) in head-restrained monkeys evokes a constant velocity eye movement. Since the PPRF receives significant projections from structures that control coordinated eye-head movements, we asked whether stimulation of the pontine reticular formation in the head-unrestrained animal generates a combined eye-head movement or only an eye movement. Microstimulation of most sites yielded a constant-velocity gaze shift executed as a coordinated eye-head movement, although eye-only movements were evoked from some sites. The eye and head contributions to the stimulationevoked movements varied across stimulation sites and were drastically different from the lawful relationship observed for visually-guided gaze shifts. These results indicate that the microstimulation activated elements that issued movement commands to the extraocular and, for most sites, neck motoneurons. In addition, the stimulation-evoked changes in gaze were similar in the head-restrained and head-unrestrained conditions despite the assortment of eye and head contributions, suggesting that the vestibuloocular reflex (VOR) gain must be near unity during the coordinated eye-head movements evoked by stimulation of the PPRF. These findings contrast the attenuation of VOR gain associated with visually-guided gaze shifts and suggest that the vestibulo-ocular pathway processes volitional and PPRF stimulation-evoked gaze shifts differently.

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Section: Eye-head Coordinationmentioning

confidence: 61%

Coordination of eye and head components of movements evoked by stimulation of the paramedian pontine reticular formation

2008

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“…Therefore, identifying Evidence supporting a within-neuron fixed threshold for saccade initiation in the FEF and SC (i.e., no significant correlation between presaccadic motor discharge rate and SRT) has been found previously in presaccadic epochs spanning the shortest time at which a neural signal can influence saccade initiation (Brown et al 2008;Hanes and Schall 1996;Paré and Hanes 2003). In the FEF this is 20 ms to 10 ms before saccade onset Büttner-Ennever et al 1988;Hanes and Schall 1996;Segraves 1992;Segraves and Goldberg 1987), and in the SC this is 18 ms to 8 ms before saccade onset (Miyashita and Hikosaka 1996;Munoz et al 1996;Munoz and Wurtz 1993). Similarly, during these epochs we found no correlation between presaccadic motor discharge rate and SRT in the FEF or the SC.…”

Section: Discussionmentioning

confidence: 81%

“…On the basis of previous physiological and anatomical studies, the latest 10-ms epoch with respect to saccade onset at which saccade initiation can be influenced by an FEF signal is 20 ms to 10 ms before saccade onset Büttner-Ennever et al 1988;Hanes and Schall 1996;Segraves 1992;Segraves and Goldberg 1987). Similarly, the latest 10-ms presaccadic epoch at which saccade initiation can be influenced by an SC signal is 18 ms to 8 ms before saccade onset (Miyashita and Hikosaka 1996;Munoz et al 1996;Munoz and Wurtz 1993). To quantify changes in FEF and SC activity in a manner comparable to previous studies (Hanes and Schall 1996;Paré and Hanes 2003), we first analyzed our results in the FEF and the SC with the respective 20 ms to 10 ms and 18 ms to 8 ms presaccadic epochs above.…”

Section: Methodsmentioning

confidence: 97%

Threshold mechanism for saccade initiation in frontal eye field and superior colliculus

Jantz

Watanabe

Everling

et al. 2013

Journal of Neurophysiology

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Jantz JJ, Watanabe M, Everling S, Munoz DP. Threshold mechanism for saccade initiation in frontal eye field and superior colliculus. J Neurophysiol 109: 2767-2780, 2013. First published March 13, 2013 doi:10.1152/jn.00611.2012-In an influential model of frontal eye field (FEF) and superior colliculus (SC) activity, saccade initiation occurs when the discharge rate of either single neurons or a population of neurons encoding a saccade motor plan reaches a threshold level of activity. Conflicting evidence exists for whether this threshold is fixed or can change under different conditions. We tested the fixed-threshold hypothesis at the single-neuron and population levels to help resolve the inconsistency between previous studies. Two rhesus monkeys performed a randomly interleaved pro-and antisaccade task in which they had to look either toward (pro) or 180°away (anti) from a peripheral visual stimulus. We isolated visuomotor (VM) and motor (M) neurons in the FEF and SC and tested three specific predictions of a fixed-threshold hypothesis. We found little support for fixed thresholds. First, correlations were never totally absent between presaccadic discharge rate and saccadic reaction time when examining a larger (plausible) temporal period. Second, presaccadic discharge rates varied markedly between saccade tasks. Third, visual responses exceeded presaccadic motor discharges for FEF and SC VM neurons. We calculated that only a remarkably strong bias for M neurons in downstream projections could render the fixed-threshold hypothesis plausible at the population level. Also, comparisons of gap vs. overlap conditions indicate that increased inhibitory tone may be associated with stability of thresholds. We propose that fixed thresholds are the exception rather than the rule in FEF and SC, and that stabilization of an otherwise variable threshold depends on task-related, inhibitory modulation. visuomotor neuron; motoneuron; prosaccade; antisaccade; inhibition THE FRONTAL EYE FIELD (FEF) and midbrain superior colliculus (SC) are brain regions that are critical for saccade initiation. Both structures contain neurons with retinotopically organized visual and motor response fields (RFs) Mohler et al. 1973;Wurtz and Goldberg 1971), and electrical microstimulation in either the FEF or the SC can elicit saccades of a specified direction and amplitude Robinson 1972;Stryker and Schiller 1975). Furthermore, permanent lesion of the FEF (Schiller and Chou 1998) or the SC (Schiller et al. 1980(Schiller et al. , 1987 produces lasting deficits in saccade initiation, and reversible inactivation of the FEF (Dias et al. 1995;Dias and Segraves 1999;Sommer and Tehovnik 1997) or the SC (Hanes and Wurtz 2001;Hikosaka and Wurtz 1985) transiently impairs production of saccades, revealed as increases in saccadic reaction time (SRT). Lesion of both structures together abolishes saccades (Schiller et al. 1979(Schiller et al. , 1980. After reversible deactivation of the SC, electrical microstimulation of the FEF cannot elicit saccades (Hanes a...

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“…Although our SSRTs are short, they are not so short as to be inconsistent with the hypothesis that fixation neurons in FEF and/or SC are involved in the stop process. For example, visual signals can reach FEF in as little as 50 ms (Hanes et al 1998;Schall 1991), signals from FEF can potentially reach SC within 2 ms (Segraves and Goldberg 1987) and SC can affect eye movements within 8 ms (Miyashita and Hikosaka 1996).…”

Section: Discussionmentioning

confidence: 99%

Behavioral Evaluation of Movement Cancellation

Walton

Gandhi²

2006

Journal of Neurophysiology

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. The countermanding saccade task has been used in many studies to investigate the neural mechanisms that underlie the decision to execute or restrain rapid eye movements. In this task, the presentation of a saccade target is sometimes followed by the appearance of a stop cue that indicates that the subject should cancel the planned movement. Performance has been modeled as a race between motor preparation and cancellation processes. The signal that reaches its activation threshold first determines whether a saccade is generated or cancelled. In these studies, an important parameter is the time required to process the stop cue, referred to as the stop signal reaction time (SSRT). The SSRT is estimated using statistical approaches, the validity of which has not been unequivocally established. A more direct measure of this parameter might be obtainable if a method was available to "unmask" the developing motor command. This can be accomplished by air-puffevoked blinks, which inhibit pontine omnipause neurons that serve as an inhibitory gate for the saccadic system. In the present study, brief puffs of air were used to elicit blinks at various times while rhesus monkeys performed a countermanding saccade task. If the developing motor command has not yet been cancelled, this should trigger a saccade. When blinks occurred between ϳ50 and 200 ms after target onset, saccades were often evoked. Saccades were rarely evoked more than ϳ70 ms after stop cue onset; this value represents a behavioral evaluation of SSRT and was comparable to the estimates obtained using standard statistical approaches. When saccades occurred near the SSRT on blink trials, they were often hypometric. Furthermore, Monte Carlo simulations were performed to model the effects of blink time on the race model. Overall, the study supports the validity of the statistical methods currently in use.

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Minimal synaptic delay in the saccadic output pathway of the superior colliculus studied in awake monkey

Cited by 59 publications

References 43 publications

Coordination of eye and head components of movements evoked by stimulation of the paramedian pontine reticular formation

Coordination of eye and head components of movements evoked by stimulation of the paramedian pontine reticular formation

Threshold mechanism for saccade initiation in frontal eye field and superior colliculus

Behavioral Evaluation of Movement Cancellation

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