Sensorimotor integration in the primate superior colliculus. I. Motor convergence

1987 ◽  
Vol 57 (1) ◽  
pp. 22-34 ◽  
Author(s):  
M. F. Jay ◽  
D. L. Sparks

Orienting movements of the eyes and head are made to both auditory and visual stimuli even though in the primary sensory pathways the locations of auditory and visual stimuli are encoded in different coordinates. This study was designed to differentiate between two possible mechanisms for sensory-to-motor transformation. Auditory and visual signals could be translated into common coordinates in order to share a single motor pathway or they could maintain anatomically separate sensory and motor routes for the initiation and guidance of orienting eye movements. The primary purpose of the study was to determine whether neurons in the superior colliculus (SC) that discharge before saccades to visual targets also discharge before saccades directed toward auditory targets. If they do, this would indicate that auditory and visual signals, originally encoded in different coordinates, have been converted into a single coordinate system and are sharing a motor circuit. Trained monkeys made saccadic eye movements to auditory or visual targets while the activity of visual-motor (V-M) cells and saccade-related burst (SRB) cells was monitored. The pattern of spike activity observed during trials in which saccades were made to visual targets was compared with that observed when comparable saccades were made to auditory targets. For most (57 of 59) V-M cells, sensory responses were observed only on visual trials. Auditory stimuli originating from the same region of space did not activate these cells. Yet, of the 72 V-M and SRB cells studied, 79% showed motor bursts prior to saccades to either auditory or visual targets. This finding indicates that visual and auditory signals, originally encoded in retinal and head-centered coordinates, respectively, have undergone a transformation that allows them to share a common efferent pathway for the generation of saccadic eye movements. Saccades to auditory targets usually have lower velocities than saccades of the same amplitude and direction made to acquire visual targets. Since fewer collicular cells are active prior to saccades to auditory targets, one determinant of saccadic velocity may be the number of collicular neurons discharging before a particular saccade.

2011 ◽  
Vol 106 (2) ◽  
pp. 690-703 ◽  
Author(s):  
Xiaobing Li ◽  
Michele A. Basso

Shifts in the location of spatial attention produce increases in the gain and sensitivity of neuronal responses to sensory stimuli. Cues to shift the line of sight have the same effect on sensory responses in a motor area involved in the control of eye movements, the superior colliculus. Evidence has shown that shifts of gaze and shifts of attention are linked, suggesting there may be similar underlying mechanisms. Here, we report on a novel way in which cues to move the eyes (top-down signals) can influence sensory responses of neurons by altering the variability of their discharge rate. We measured the spatial tuning of superior colliculus neuronal activity in trials with cues to either make or withhold saccadic eye movements. We found that tuning curve widths both increased and decreased, but that the information conveyed by the neuronal discharge about the stimulus increased with a cue to make a saccade. The increase in information resulted partly from a decrease in trial-to-trial variability of neuronal discharges for stimuli located at the flanks of the tuning curves rather than from increases in the discharge rate for stimuli located at the peak of the tuning curves. This result is consistent with theoretical work and provides a novel way for cognitive signals to influence sensory responses within motor regions of the brain.


2012 ◽  
Vol 108 (10) ◽  
pp. 2653-2667 ◽  
Author(s):  
Jan Churan ◽  
Daniel Guitton ◽  
Christopher C. Pack

Saccades are useful for directing the high-acuity fovea to visual targets that are of behavioral relevance. The selection of visual targets for eye movements involves the superior colliculus (SC), where many neurons respond to visual stimuli. Many of these neurons are also activated before and during saccades of specific directions and amplitudes. Although the role of the SC in controlling eye movements has been thoroughly examined, far less is known about the nature of the visual responses in this area. We have, therefore, recorded from neurons in the intermediate layers of the macaque SC, while using a sparse-noise mapping procedure to obtain a detailed characterization of the spatiotemporal structure of visual receptive fields. We find that SC responses to flashed visual stimuli start roughly 50 ms after the onset of the stimulus and last for on average ∼70 ms. About 50% of these neurons are strongly suppressed by visual stimuli flashed at certain locations flanking the excitatory center, and the spatiotemporal pattern of suppression exerts a predictable influence on the timing of saccades. This suppression may, therefore, contribute to the filtering of distractor stimuli during target selection. We also find that saccades affect the processing of visual stimuli by SC neurons in a manner that is quite similar to the saccadic suppression and postsaccadic enhancement that has been observed in the cortex and in perception. However, in contrast to what has been observed in the cortex, decreased visual sensitivity was generally associated with increased firing rates, while increased sensitivity was associated with decreased firing rates. Overall, these results suggest that the processing of visual stimuli by SC receptive fields can influence oculomotor behavior and that oculomotor signals originating in the SC can shape perisaccadic visual perception.


1977 ◽  
Vol 40 (1) ◽  
pp. 74-94 ◽  
Author(s):  
C. W. Mohler ◽  
R. H. Wurtz

1. We studied the effect of lesions placed in striate cortex or superior colliculus on the detection of visual stimuli and the accuracy of saccadic eye movements. The monkeys (Macaca mulatta) first learned to respond to a 0.25 degrees spot of light flashed for 150-200 ms in one part of the visual field while they were fixating in order to determine if they could detect the light. The monkeys also learned in a different task to make a saccade to the spot of light when the fixation point went out, and the accuracy of the saccades was measured. 2. Following a unilateral partial ablation of the striate cortex in two monkeys they could not detect the spot of light in the resulting scotoma or saccade to it. The deficit was only relative; if we increased the brightness of the stimulus from the usual 11 cd/m2 to 1,700 cd/m2 against a background of 1 cd/m2 the monkeys were able to detect and to make a saccade to the spot of light. 3. Following about 1 mo of practice on the detection and saccade tasks, the monkeys recovered the ability to detect the spots of light and to make saccades to them without gross errors (saccades made beyond an area of +/-3 average standard deviations). Lowering the stimulus intensity reinstated both the detection and saccadic errors...


2012 ◽  
Vol 107 (9) ◽  
pp. 2442-2452 ◽  
Author(s):  
Husam A. Katnani ◽  
A. J. Van Opstal ◽  
Neeraj J. Gandhi

Population coding is a ubiquitous principle in the nervous system for the proper control of motor behavior. A significant amount of research is dedicated to studying population activity in the superior colliculus (SC) to investigate the motor control of saccadic eye movements. Vector summation with saturation (VSS) has been proposed as a mechanism for how population activity in the SC can be decoded to generate saccades. Interestingly, the model produces different predictions when decoding two simultaneous populations at high vs. low levels of activity. We tested these predictions by generating two simultaneous populations in the SC with high or low levels of dual microstimulation. We also combined varying levels of stimulation with visually induced activity. We found that our results did not perfectly conform to the predictions of the VSS scheme and conclude that the simplest implementation of the model is incomplete. We propose that additional parameters to the model might account for the results of this investigation.


1996 ◽  
Vol 76 (3) ◽  
pp. 1439-1456 ◽  
Author(s):  
P. Mazzoni ◽  
R. M. Bracewell ◽  
S. Barash ◽  
R. A. Andersen

1. The lateral intraparietal area (area LIP) of the monkey's posterior parietal cortex (PPC) contains neurons that are active during saccadic eye movements. These neurons' activity includes visual and saccade-related components. These responses are spatially tuned and the location of a neuron's visual receptive field (RF) relative to the fovea generally overlaps its preferred saccade amplitude and direction (i.e., its motor field, MF). When a delay is imposed between the presentation of a visual stimulus and a saccade made to its location (memory saccade task), many LIP neurons maintain elevated activity during the delay (memory activity, M), which appears to encode the metrics of the next intended saccadic eye movements. Recent studies have alternatively suggested that LIP neurons encode the locations of visual stimuli regardless of where the animal intends to look. We examined whether the M activity of LIP neurons specifically encodes movement intention or the locations of recent visual stimuli, or a combination of both. In the accompanying study, we investigated whether the intended-movement activity reflects changes in motor plan. 2. We trained monkeys (Macaca mulatta) to memorize the locations of two visual stimuli and plan a sequence of two saccades, one to each remembered target, as we recorded the activity of single LIP neurons. Two targets were flashed briefly while the monkey maintained fixation; after a delay the fixation point was extinguished, and the monkey made two saccades in sequence to each target's remembered location, in the order in which the targets were presented. This "delayed double saccade" (DDS) paradigm allowed us to dissociate the location of visual stimulation from the direction of the planned saccade and thus distinguish neuronal activity related to the target's location from activity related to the saccade plan. By imposing a delay, we eliminated the confounding effect of any phasic responses coincident with the appearance of the stimulus and with the saccade. 3. We arranged the two visual stimuli so that in one set of conditions at least the first one was in the neuron's visual RF, and thus the first saccade was in the neuron's motor field (MF). M activity should be high in these conditions according to both the sensory memory and motor plan hypotheses. In another set of conditions, the second stimulus appeared in the RF but the first one was presented outside the RF, instructing the monkey to plan the first saccade away from the neuron's MF. If the M activity encodes the motor plan, it should be low in these conditions, reflecting the plan for the first saccade (away from the MF). If it is a sensory trace of the stimulus' location, it should be high, reflecting stimulation of the RF by the second target. 4. We tested 49 LIP neurons (in 3 hemispheres of 2 monkeys) with M activity on the DDS task. Of these, 38 (77%) had M activity related to the next intended saccade. They were active in the delay period, as expected, if the first saccade was in their preferred direction. They were less active or silent if the next saccade was not in their preferred direction, even when the second stimulus appeared in their RF. 5. The M activity of 8 (16%) of the remaining neurons specifically encoded the location of the most recent visual stimulus. Their firing rate during the delay reflected stimulation of the RF independently of the saccade being planned. The remaining 3 neurons had M activity that did not consistently encode either the next saccade or the stimulus' location. 6. We also recorded the activity of a subset of neurons (n = 38) in a condition in which no stimulus appeared in a neuron's RF, but the second saccade was in the neuron's MF. In this case the majority of neurons tested (23/38, 60%) became active in the period between the first and second saccade, even if neither stimulus had appeared in their RF. Moreover, this activity appeared only after the first saccade had started in all but two of


1991 ◽  
Vol 6 (1) ◽  
pp. 3-13 ◽  
Author(s):  
James T. McIlwain

AbstractThis paper reviews evidence that the superior colliculus (SC) of the midbrain represents visual direction and certain aspects of saccadic eye movements in the distribution of activity across a population of cells. Accurate and precise eye movements appear to be mediated, in part at least, by cells of the SC that have large sensory receptive fields and/or discharge in association with a range of saccades. This implies that visual points or saccade targets are represented by patches rather than points of activity in the SC. Perturbation of the pattern of collicular discharge by focal inactivation modifies saccade amplitude and direction in a way consistent with distributed coding. Several models have been advanced to explain how such a code might be implemented in the colliculus. Evidence related to these hypotheses is examined and continuing uncertainties are identified.


2016 ◽  
Vol 116 (6) ◽  
pp. 2541-2549 ◽  
Author(s):  
John R. Economides ◽  
Daniel L. Adams ◽  
Jonathan C. Horton

The superior colliculus is a major brain stem structure for the production of saccadic eye movements. Electrical stimulation at any given point in the motor map generates saccades of defined amplitude and direction. It is unknown how this saccade map is affected by strabismus. Three macaques were raised with exotropia, an outwards ocular deviation, by detaching the medial rectus tendon in each eye at age 1 mo. The animals were able to make saccades to targets with either eye and appeared to alternate fixation freely. To probe the organization of the superior colliculus, microstimulation was applied at multiple sites, with the animals either free-viewing or fixating a target. On average, microstimulation drove nearly conjugate saccades, similar in both amplitude and direction but separated by the ocular deviation. Two monkeys showed a pattern deviation, characterized by a systematic change in the relative position of the two eyes with certain changes in gaze angle. These animals' saccades were slightly different for the right eye and left eye in their amplitude or direction. The differences were consistent with the animals' underlying pattern deviation, measured during static fixation and smooth pursuit. The tectal map for saccade generation appears to be normal in strabismus, but saccades may be affected by changes in the strabismic deviation that occur with different gaze angles.


1997 ◽  
Vol 17 (20) ◽  
pp. 7941-7953 ◽  
Author(s):  
M. Concetta Morrone ◽  
John Ross ◽  
David C. Burr

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