Saccadic command signals in the superior colliculus: implications for sensorimotor transformations

1988 ◽  
Vol 66 (5) ◽  
pp. 527-531 ◽  
Author(s):  
David L. Sparks

Recent findings concerning the anatomical and functional organization of the deep division of the primate superior colliculus are summarized. These data are interpreted as supporting the hypothesis that the deeper layers of the superior colliculus are organized in motor, rather than sensory, coordinates. According to this hypothesis, a dynamic remapping of sensory signals is required for interfacing with the map of motor error space contained in the superior colliculus

2019 ◽  
Author(s):  
Corentin Massot ◽  
Uday K. Jagadisan ◽  
Neeraj J. Gandhi

AbstractThe superior colliculus (SC) is an excellent substrate to study functional organization of sensorimotor transformations. We used linear multi-contact array recordings to analyze the spatial and temporal properties of population activity along the SC dorsoventral axis during delayed saccade tasks. During the visual epoch, information appeared first in dorsal layers and systematically later in ventral layers. In the ensuing delay period, the laminar organization of low-spiking rate activity matched that of the visual epoch. During the pre-saccadic epoch, spiking activity emerged first in a more ventral layer, ∼100ms before saccade onset. This buildup of activity appeared later on nearby neurons situated both dorsally and ventrally, culminating in a synchronous burst across the dorsoventral axis, ∼28ms before saccade onset. Stimulation of individual contacts on the laminar probe produced saccades of similar vectors. Collectively, the results reveal a principled spatiotemporal organization of SC population activity underlying sensorimotor transformation for the control of gaze.


2002 ◽  
Vol 87 (2) ◽  
pp. 679-695 ◽  
Author(s):  
Robijanto Soetedjo ◽  
Chris R. S. Kaneko ◽  
Albert F. Fuchs

There is general agreement that saccades are guided to their targets by means of a motor error signal, which is produced by a local feedback circuit that calculates the difference between desired saccadic amplitude and an internal copy of actual saccadic amplitude. Although the superior colliculus (SC) is thought to provide the desired saccadic amplitude signal, it is unclear whether the SC resides in the feedback loop. To test this possibility, we injected muscimol into the brain stem region containing omnipause neurons (OPNs) to slow saccades and then determined whether the firing of neurons at different sites in the SC was altered. In 14 experiments, we produced saccadic slowing while simultaneously recording the activity of a single SC neuron. Eleven of the 14 neurons were saccade-related burst neurons (SRBNs), which discharged their most vigorous burst for saccades with an optimal amplitude and direction (optimal vector). The optimal directions for the 11 SRBNs ranged from nearly horizontal to nearly vertical, with optimal amplitudes between 4 and 17°. Although muscimol injections into the OPN region produced little change in the optimal vector, they did increase mean saccade duration by 25 to 192.8% and decrease mean saccade peak velocity by 20.5 to 69.8%. For optimal vector saccades, both the acceleration and deceleration phases increased in duration. However, during 10 of 14 experiments, the duration of deceleration increased as fast as or faster than that of acceleration as saccade duration increased, indicating that most of the increase in duration occurred during the deceleration phase. SRBNs in the SC changed their burst duration and firing rate concomitantly with changes in saccadic duration and velocity, respectively. All SRBNs showed a robust increase in burst duration as saccadic duration increased. Five of 11 SRBNs also exhibited a decrease in burst peak firing rate as saccadic velocity decreased. On average across the neurons, the number of spikes in the burst was constant. There was no consistent change in the discharge of the three SC neurons that did not exhibit bursts with saccades. Our data show that the SC receives feedback from downstream saccade-related neurons about the ongoing saccades. However, the changes in SC firing produced in our study do not suggest that the feedback is involved with producing motor error. Instead, the feedback seems to be involved with regulating the duration of the discharge of SRBNs so that the desired saccadic amplitude signal remains present throughout the saccade.


2015 ◽  
Vol 114 (2) ◽  
pp. 978-988 ◽  
Author(s):  
Elizabeth A. Stubblefield ◽  
John A. Thompson ◽  
Gidon Felsen

The superior colliculus (SC) plays a critical role in orienting movements, in part by integrating modulatory influences on the sensorimotor transformations it performs. Many species exhibit a robust brain stem cholinergic projection to the intermediate and deep layers of the SC arising mainly from the pedunculopontine tegmental nucleus (PPTg), which may serve to modulate SC function. However, the physiological effects of this input have not been examined in vivo, preventing an understanding of its functional role. Given the data from slice experiments, cholinergic input may have a net excitatory effect on the SC. Alternatively, the input could have mixed effects, via activation of inhibitory neurons within or upstream of the SC. Distinguishing between these possibilities requires in vivo experiments in which endogenous cholinergic input is directly manipulated. Here we used anatomical and optogenetic techniques to identify and selectively activate brain stem cholinergic terminals entering the intermediate and deep layers of the awake mouse SC and recorded SC neuronal responses. We first quantified the pattern of the cholinergic input to the mouse SC, finding that it was predominantly localized to the intermediate and deep layers. We then found that optogenetic stimulation of cholinergic terminals in the SC significantly increased the activity of a subpopulation of SC neurons. Interestingly, cholinergic input had a broad range of effects on the magnitude and timing of SC responses, perhaps reflecting both monosynaptic and polysynaptic innervation. These findings begin to elucidate the functional role of this cholinergic projection in modulating the processing underlying sensorimotor transformations in the SC.


1995 ◽  
Vol 73 (4) ◽  
pp. 1724-1728 ◽  
Author(s):  
A. A. Kustov ◽  
D. L. Robinson

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.


1994 ◽  
Vol 72 (6) ◽  
pp. 2754-2770 ◽  
Author(s):  
E. L. Keller ◽  
J. A. Edelman

1. We recorded the spatial and temporal dynamics of saccade-related burst neurons (SRBNs) found in the intermediate layers of the superior colliculus (SC) in the alert, behaving monkey. These burst cells are normally the first neurons recorded during radially directed microelectrode penetrations of the SC after the electrode has left the more dorsally situated visual layers. They have spatially delimited movement fields whose centers describe the well-studied motor map of the SC. They have a rather sharp, saccade-locked burst of activity that peaks just before saccade onset and then declines steeply during the saccade. Many of these cells, when recorded during saccade trials, also have an early, transient visual response and an irregular prelude of presaccadic activity. 2. Because saccadic eye movements normally have very stereotyped durations and velocity trajectories that vary systematically with saccade size, it has been difficult in the past to establish quantitatively whether the activity of SRBNs temporally codes dynamic saccadic control signals, e.g., dynamic motor error or eye velocity, where dynamic motor error is defined as a signal proportional to the instantaneous difference between desired final eye position and the actual eye position during a saccade. It has also not been unequivocally established whether SRBNs participate in an organized spatial shift of ensemble activity in the intermediate layers of the SC during saccadic eye movements. 3. To address these issues, we studied the activity of SRBNs using an interrupted saccade paradigm. Saccades were interrupted with pulsatile electrical stimulation through a microelectrode implanted in the omnipauser region of the brain stem while recordings were made simultaneously from single SRBNs in the SC. 4. Shortly after the beginning of the stimulation (which was electronically triggered at saccade onset), the eyes decelerated rapidly and stopped completely. When the high-frequency (typically 300-400 pulses per second) stimulation was terminated (average duration 12 ms), the eye movement was reinitiated and a resumed saccade was made accurately to the location of the target. 5. When we recorded from SRBNs in the more caudal colliculus, which were active for large saccades, cell discharge was powerfully and rapidly suppressed by the stimulation (average latency = 3.8 ms). Activity in the same cells started again just before the onset of the resumed saccade and continued during this saccade even though it has a much smaller amplitude than would normally be associated with significant discharge for caudal SC cells.(ABSTRACT TRUNCATED AT 400 WORDS)


1984 ◽  
Vol 51 (3) ◽  
pp. 407-431 ◽  
Author(s):  
R. D. Mooney ◽  
S. E. Fish ◽  
R. W. Rhoades

A series of anatomical (autoradiographic and horseradish peroxidase, HRP) and electrophysiological experiments were carried out to determine the organization of the pathway from the superior colliculus (SC) to the lateral posterior nucleus (LP) in the hamster. Small, electrophoretic HRP deposits restricted to LP labeled numerous cells in both the ipsilateral and contralateral colliculus. Over 95% of the labeled cells were located in the lower one-half of the stratum griseum superficiale (SGS) and the upper stratum opticum (SO). A number of different morphological cell types contributed axons to the tecto-LP pathway. The receptive-field properties of antidromically activated tecto-LP neurons were delineated using extracellular single-unit recording techniques. Ninety-eight percent of the tecto-LP cells recorded were isolated in the SGS and SO. All tecto-LP cells responded more vigorously to moving than to flashed stimuli, one-third were directionally selective, and one-third exhibited some degree of speed selectivity. The responses of tecto-LP neurons did not differ appreciably from those of superficial layer collicular cells that could not be antidromically activated by LP shocks. Small pressure injections or electrophoretic deposits of [3H]leucine into sites with known retinotopy in the superficial collicular laminae were used to determine whether or not the tecto-LP projection in hamster was topographically organized. Injections anywhere in the SGS and SO yielded dense label in almost all of the caudal (LPc) and rostrolateral (LPrl) subnuclei of LP, ipsilaterally, and sparser labeling in these same subnuclei, contralaterally. No injection produced significant labeling in the rostromedial (LPrm) subnucleus. Our autoradiographic data gave no indication of any topographic order in the tecto-LP projection. Electrophysiological methods were also used to map the tecto-LP projection. Multiple stimulating microelectrodes were positioned at physiologically defined sites in the SGS, and single cells were recorded in LP, ipsilaterally. Threshold currents for activation of LP cells from different collicular sites were then compared with the angular separation of SC and LP receptive-field centers. No significant correlation between these two variables was noted, again indicating a lack of topographic organization in the tecto-LP projection. The receptive-field properties of individual LP neurons (n = 211) were also assessed and correlated with subnuclear location and responsivity to SC shocks.(ABSTRACT TRUNCATED AT 400 WORDS)


2018 ◽  
Vol 115 (38) ◽  
pp. E8987-E8995 ◽  
Author(s):  
Yoshiko Kojima ◽  
Robijanto Soetedjo

When movements become dysmetric, the resultant motor error induces a plastic change in the cerebellum to correct the movement, i.e., motor adaptation. Current evidence suggests that the error signal to the cerebellum is delivered by complex spikes originating in the inferior olive (IO). To prove a causal link between the IO error signal and motor adaptation, several studies blocked the IO, which, unfortunately, affected not only the adaptation but also the movement itself. We avoided this confound by inactivating the source of an error signal to the IO. Several studies implicate the superior colliculus (SC) as the source of the error signal to the IO for saccade adaptation. When we inactivated the SC, the metrics of the saccade to be adapted were unchanged, but saccade adaptation was impaired. Thus, an intact rostral SC is necessary for saccade adaptation. Our data provide experimental evidence for the cerebellar learning theory that requires an error signal to drive motor adaptation.


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