Gaze position effects and position-dependent motor tuning from primate superior colliculus (SC) neurons during head-unrestrained visually guided movements

AbstractMicrosaccades are overwhelmingly described as involuntary eye movements. Here we show in both human subjects and monkeys that individual microsaccades of any direction can easily be triggered: (1) “on demand”, based on an arbitrary instruction, (2) without any special training, (3) without visual guidance by a stimulus, and (4) in a spatially and temporally accurate manner. Subjects voluntarily generated instructed “memory-guided” microsaccades readily, and similarly to how they made normal visually-guided ones. In two monkeys, we also observed midbrain superior colliculus neurons that exhibited movement-related activity bursts exclusively for memory-guided microsaccades, but not for similarly-sized visually-guided movements. Our results demonstrate behavioral and neural evidence for voluntary control over individual microsaccades, supporting recently discovered functional contributions of individual microsaccade generation to visual performance alterations and covert visual selection.

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Nonstationary properties of the saccadic system: new constraints on models of saccadic control

Journal of Neurophysiology ◽

10.1152/jn.1995.73.1.431 ◽

1995 ◽

Vol 73 (1) ◽

pp. 431-435 ◽

Cited By ~ 45

Author(s):

M. J. Nichols ◽

D. L. Sparks

Keyword(s):

Superior Colliculus ◽

Time Constant ◽

Time Course ◽

Visually Guided ◽

Exponential Time ◽

Classic Model ◽

Saccadic System ◽

Visually Guided Movements ◽

Displacement Model

1. We tested the predictions of two models of the saccadic burst generator by electrically stimulating sites in primate superior colliculus (SC) immediately following visually guided movements. 2. The amplitude and direction of stimulated saccades depend systematically on the amplitude and direction of preceding visually guided saccades, and that effect decays exponentially with a time constant of approximately 45 ms. The saccadic system, then, displays an amplitude-dependent non-stationarity that follows an exponential time course during the intersaccadic interval (ISI). 3. These results are consistent with a variant of the eye displacement model proposed by Jurgens et al. but not with Robinson's classic model of the burst generator. Moreover, since all models of saccadic control must predict either stationary or nonstationary behavior during the ISI, these results provide a powerful new constraint on those models. 4. Finally, the success of the displacement model in accounting for our data suggests a new explanation for the results of colliding saccade experiments.

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Effects of low-frequency stimulation of the superior colliculus on spontaneous and visually guided saccades

Journal of Neurophysiology ◽

10.1152/jn.1993.69.3.953 ◽

1993 ◽

Vol 69 (3) ◽

pp. 953-964 ◽

Cited By ~ 43

Author(s):

P. W. Glimcher ◽

D. L. Sparks

Keyword(s):

Superior Colliculus ◽

Time Course ◽

Low Frequency ◽

Arbitrary Point ◽

Visually Guided ◽

Spontaneous Movements ◽

Low Frequency Stimulation ◽

Frequency Stimulation ◽

Stimulation Current ◽

Stimulation Of

1. The first experiment of this study determined the effects of low-frequency stimulation of the monkey superior colliculus on spontaneous saccades in the dark. Stimulation trains, subthreshold for eliciting short-latency fixed-vector saccades, were highly effective at biasing the metrics (direction and amplitude) of spontaneous movements. During low-frequency stimulation, the distribution of saccade metrics was biased toward the direction and amplitude of movements induced by suprathreshold stimulation of the same collicular location. 2. Low-frequency stimulation biased the distribution of saccade metrics but did not initiate movements. The distribution of intervals between stimulation onset and the onset of the next saccade did not differ significantly from the distribution of intervals between an arbitrary point in time and the onset of the next saccade under unstimulated conditions. 3. Results of our second experiment indicate that low-frequency stimulation also influenced the metrics of visually guided saccades. The magnitude of the stimulation-induced bias increased as stimulation current or frequency was increased. 4. The time course of these effects was analyzed by terminating stimulation immediately before, during, or after visually guided saccades. Stimulation trains terminated at the onset of a movement were as effective as stimulation trains that continued throughout the movement. No effects were observed if stimulation ended 40–60 ms before the movement began. 5. These results show that low-frequency collicular stimulation can influence the direction and amplitude of spontaneous or visually guided saccades without initiating a movement. These data are compatible with the hypothesis that the collicular activity responsible for specifying the horizontal and vertical amplitude of a saccade differs from the type of collicular activity that initiates a saccade.

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Effects of Local Nicotinic Activation of the Superior Colliculus on Saccades in Monkeys

Journal of Neurophysiology ◽

10.1152/jn.00558.2004 ◽

2005 ◽

Vol 93 (1) ◽

pp. 519-534 ◽

Cited By ~ 21

Author(s):

Masayuki Watanabe ◽

Yasushi Kobayashi ◽

Yuka Inoue ◽

Tadashi Isa

Keyword(s):

Superior Colliculus ◽

Reaction Times ◽

Low Frequency ◽

Visually Guided ◽

Population Activity ◽

Affected Area ◽

Movement Field ◽

Neural Interactions ◽

Restricted Region

To examine the role of competitive and cooperative neural interactions within the intermediate layer of superior colliculus (SC), we elevated the basal SC neuronal activity by locally injecting a cholinergic agonist nicotine and analyzed its effects on saccade performance. After microinjection, spontaneous saccades were directed toward the movement field of neurons at the injection site (affected area). For visually guided saccades, reaction times were decreased when targets were presented close to the affected area. However, when visual targets were presented remote from the affected area, reaction times were not increased regardless of the rostrocaudal level of the injection sites. The endpoints of visually guided saccades were biased toward the affected area when targets were presented close to the affected area. After this endpoint effect diminished, the trajectories of visually guided saccades remained modestly curved toward the affected area. Compared with the effects on endpoints, the effects on reaction times were more localized to the targets close to the affected area. These results are consistent with a model that saccades are triggered by the activities of neurons within a restricted region, and the endpoints and trajectories of the saccades are determined by the widespread population activity in the SC. However, because increased reaction times were not observed for saccades toward targets remote from the affected area, inhibitory interactions in the SC may not be strong enough to shape the spatial distribution of the low-frequency preparatory activities in the SC.

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The event related potential technique and microstate analysis of memory guided and visually guided movements.

Journal of Vision ◽

10.1167/14.10.303 ◽

2014 ◽

Vol 14 (10) ◽

pp. 303-303

Author(s):

D. Cheng ◽

K. Fjeld ◽

G. Binsted

Keyword(s):

Event Related Potential ◽

Visually Guided ◽

Visually Guided Movements ◽

Microstate Analysis

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Is proprioception calibrated during visually guided movements?

Experimental Brain Research ◽

10.1007/s00221-005-0063-5 ◽

2005 ◽

Vol 167 (2) ◽

pp. 292-296 ◽

Cited By ~ 34

Author(s):

Pierre-Michel Bernier ◽

Romeo Chua ◽

Ian M. Franks

Keyword(s):

Visually Guided ◽

Visually Guided Movements

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Injection of Nicotine Into the Superior Colliculus Facilitates Occurrence of Express Saccades in Monkeys

Journal of Neurophysiology ◽

10.1152/jn.1999.82.3.1642 ◽

1999 ◽

Vol 82 (3) ◽

pp. 1642-1646 ◽

Cited By ~ 47

Author(s):

Hiroshi Aizawa ◽

Yasushi Kobayashi ◽

Masaru Yamamoto ◽

Tadashi Isa

Keyword(s):

Superior Colliculus ◽

Nicotinic Acetylcholine Receptors ◽

Acetylcholine Receptors ◽

Marked Change ◽

Major Change ◽

Visually Guided ◽

Express Saccades ◽

Macaque Monkeys ◽

The Relationship

To clarify the role of cholinergic inputs to the intermediate layer of the superior colliculus (SC), we examined the effect of microinjection of nicotine into the SC on visually guided saccades in macaque monkeys. After injection of 0.4–2 μl of 1–100 mM nicotine into the SC, frequency of extremely short latency saccades (express saccades; reaction time = 70–120 ms) dramatically increased, for the saccades the direction and amplitude of which were represented at the location of the injection site on the collicular map. However, no marked change was observed for the relationship between the peak velocities and the amplitudes of saccades. These results suggested that activation of nicotinic acetylcholine receptors in the SC can facilitate initiation but causes no major change in dynamics of visually guided saccades.

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Modified saccades evoked by stimulation of the macaque superior colliculus account for properties of the resettable integrator

Journal of Neurophysiology ◽

10.1152/jn.1995.73.4.1724 ◽

1995 ◽

Vol 73 (4) ◽

pp. 1724-1728 ◽

Cited By ~ 29

Author(s):

A. A. Kustov ◽

D. L. Robinson

Keyword(s):

Superior Colliculus ◽

Pulse Signal ◽

Good Evidence ◽

Visually Guided ◽

Saccadic System ◽

Time Period ◽

Motor Error ◽

Stimulation Of

1. Models of the saccadic system propose that there is an integration of the pulse signal, and there is good evidence that the integrator is reset gradually (Nichols and Sparks 1994, 1995). Other studies of the superior collicular contribution to the saccadic system have proposed a sensory, not motor, nature for its signal. 2. To test experimentally the resetting of the integrator and the nature of the collicular signal, we electrically stimulated the superior colliculus during periods of fixation and during the course of visually guided saccades. Trains of stimuli which were presented during periods of fixation evoked saccades with fixed vectors. Identical stimulation at the beginning of a visually guided saccade evoked saccades whose direction was rotated and amplitude extended from the fixed vector. The direction of the rotation was opposite that of the visually guided saccade, and the magnitude of this rotation could be as large as 80 degrees. 3. Stimulation which was applied at progressively later times during the visually guided saccade, evoked saccades with progressively smaller rotations and progressively less elongations. The time period during which saccades were modified persisted beyond the end of the visually guided saccade, when the eyes were stationary. Thus, we confirm the previous findings (Nichols and Sparks 1994, 1995; Robinson, 1972), that the end of the saccade is not a period of quiescence within the oculomotor pathways. 4. Our results confirm that the resetting of the integration of the saccade signal is gradual rather than abrupt. Furthermore, these data suggest that the superior colliculus signals a motor error.

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