Spatial and temporal visual properties of the neurons in the intermediate layers of the superior colliculus

2009 ◽  
Vol 454 (1) ◽  
pp. 76-80 ◽  
Author(s):  
Zita Márkus ◽  
Antal Berényi ◽  
Zsuzsanna Paróczy ◽  
Marek Wypych ◽  
Wioletta J. Waleszczyk ◽  
...  
2020 ◽  
Vol 14 ◽  
Author(s):  
Hannah F. Waguespack ◽  
Brittany L. Aguilar ◽  
Ludise Malkova ◽  
Patrick A. Forcelli

The deep and intermediate layers of the superior colliculus (DLSC) respond to visual, auditory, and tactile inputs and act as a multimodal sensory association area. In turn, activity in the DLSC can drive orienting and avoidance responses—such as saccades and head and body movements—across species, including in rats, cats, and non-human primates. As shown in rodents, DLSC also plays a role in regulating pre-pulse inhibition (PPI) of the acoustic startle response (ASR), a form of sensorimotor gating. DLSC lesions attenuate PPI and electrical stimulation of DLSC inhibits the startle response. While the circuitry mediating PPI is well-characterized in rodents, less is known about PPI regulation in primates. Two recent studies from our labs reported a species difference in the effects of pharmacological inhibition of the basolateral amygdala and substantia nigra pars reticulata (SNpr) on PPI between rats and macaques: in rats, inhibition of these structures decreased PPI, while in macaques, it increased PPI. Given that the SNpr sends direct inhibitory projections to DLSC, we next sought to determine if this species difference was similarly evident at the level of DLSC. Here, we transiently inactivated DLSC in four rhesus macaques by focal microinfusion of the GABAA receptor agonist muscimol. Similar to findings reported in rodents, we observed that bilateral inhibition of the DLSC in macaques significantly disrupted PPI. The impairment was specific to the PPI as the ASR itself was not affected. These results indicate that our previously reported species divergence at the level of the SNpr is not due to downstream differences at the level of the DLSC. Species differences at the level of the SNpr and basolateral amygdala emphasize the importance of studying the underlying circuitry in non-human primates, as impairment in PPI has been reported in several disorders in humans, including schizophrenia, autism, and PTSD.


2001 ◽  
Vol 86 (2) ◽  
pp. 676-691 ◽  
Author(s):  
Jay A. Edelman ◽  
Michael E. Goldberg

Neurons in the intermediate layers of the superior colliculus respond to visual targets and/or discharge immediately before and during saccades. These visual and motor responses have generally been considered independent, with the visual response dependent on the nature of the stimulus, and the saccade-related activity related to the attributes of the saccade, but not to how the saccade was elicited. In these experiments we asked whether saccade-related discharge in the superior colliculus depended on whether the saccade was directed to a visual target. We recorded extracellular activity of neurons in the intermediate layers of the superior colliculus of three rhesus monkeys during saccades in tasks in which we varied the presence or absence of a visual target and the temporal delays between the appearance and disappearance of a target and saccade initiation. Across our sample of neurons ( n = 64), discharge was highest when a saccade was made to a still-present visual target, regardless of whether the target had recently appeared or had been present for several hundred milliseconds. Discharge was intermediate when the target had recently disappeared and lowest when the target had never appeared during that trial. These results are consistent with the hypothesis that saccade-related discharge decreases as the time between the target disappearance and saccade initiation increases. Saccade velocity was also higher for saccades to visual targets, and correlated on a trial-by-trial basis with perisaccadic discharge for many neurons. However, discharge of many neurons was dependent on task but independent of saccade velocity, and across our sample of neurons, saccade velocity was higher for saccades made immediately after target appearance than would be predicted by discharge level. A tighter relationship was found between saccade precision and perisaccadic discharge. These findings suggest that just as the purpose of the saccadic system in primates is to drive the fovea to a visual target, presaccadic motor activity in the superior colliculus is most intense when such a target is actually present. This enhanced activity may, itself, contribute to the enhanced performance of the saccade system when the saccade is made to a real visual target.


2014 ◽  
Vol 40 (2) ◽  
pp. 2329-2343 ◽  
Author(s):  
Penphimon Phongphanphanee ◽  
Robert A. Marino ◽  
Katsuyuki Kaneda ◽  
Yuchio Yanagawa ◽  
Douglas P. Munoz ◽  
...  

1976 ◽  
Vol 39 (4) ◽  
pp. 722-744 ◽  
Author(s):  
C. W. Mohler ◽  
R. H. Wurtz

1. We investigated the characteristics of cells in the intermediate layers of the superior colliculus that increase their rate of discharge before saccadic eye movements. Eye movements were repeatedly elicited by training rhesus monkeys to fixate on a spot of light and to make saccades to other spots of light when the fixation spot was turned off. 2. The eye movement cells showed consistent variations with their depth within the colliculus. The onset of the cell discharge led the eye movement by less time and the duration of the discharge was shorter as the cell was located closer to the dorsal edge of the intermediate layers. The movements fields (that area of the visual field where a saccade into the area is preceded by a burst of cell discharges) of each successive cell also became smaller as the cells were located more dorsally. The profile of peak discharge frequency remained fairly flat throughout the movement field of the cells regardless of depth of the cell within the colliculus. 3. A new type of eye movement-related cell has been found which usually lies at the border between the superficial and intermediate layers. This cell type, the visually triggered movement cell, increased its rate of discharge before saccades made to a visual stimulus but not before spontaneous saccades of equal amplitude made in the light or the dark. A vigorous discharge of these cells before an eye movement was dependent on the presence of a visual target; the cells seemed to combine the visual input of superficial layer cells and the movement-related input of the intermediate layer cells. The size of the movement fields of these cells were about the same size as the visual fields of superficial layer cells just above them...


2015 ◽  
Vol 113 (5) ◽  
pp. 1414-1422 ◽  
Author(s):  
Joo-Hyun Song ◽  
Robert M. McPeek

We recently demonstrated that inactivation of the primate superior colliculus (SC) causes a deficit in target selection for arm-reaching movements when the reach target is located in the inactivated field (Song JH, Rafal RD, McPeek RM. Proc Natl Acad Sci USA 108: E1433–E1440, 2011). This is consistent with the notion that the SC is part of a general-purpose target selection network beyond eye movements. To understand better the role of SC activity in reach target selection, we examined how individual SC neurons in the intermediate layers discriminate a reach target from distractors. Monkeys reached to touch a color oddball target among distractors while maintaining fixation. We found that many SC neurons robustly discriminate the goal of the reaching movement before the onset of the reach even though no saccade is made. To identify these cells in the context of conventional SC cell classification schemes, we also recorded visual, delay-period, and saccade-related responses in a delayed saccade task. On average, SC cells that discriminated the reach target from distractors showed significantly higher visual and delay-period activity than nondiscriminating cells, but there was no significant difference in saccade-related activity. Whereas a majority of SC neurons that discriminated the reach target showed significant delay-period activity, all nondiscriminating cells lacked such activity. We also found that some cells without delay-period activity did discriminate the reach target from distractors. We conclude that the majority of intermediate-layer SC cells discriminate a reach target from distractors, consistent with the idea that the SC contains a priority map used for effector-independent target selection.


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)


1980 ◽  
Vol 38 (1) ◽  
Author(s):  
G. Rizzolatti ◽  
H.A. Buchtel ◽  
R. Camarda ◽  
C. Scandolara

1995 ◽  
Vol 73 (6) ◽  
pp. 2334-2348 ◽  
Author(s):  
D. P. Munoz ◽  
R. H. Wurtz

1. In the companion paper we described two classes of cells in the monkey superior colliculus (SC) that were related to saccade generation, buildup cells and burst cells, which fell into two functional sublayers within the intermediate layers of the SC. Fixation cells in the rostral SC were deemed to be part of the buildup cell layer. The buildup cells had several characteristics in common with cells in the cat described as having a "hill of activity" moving across the SC, but the burst cells had no such characteristics. In this paper we further investigate whether there is evidence for such a moving hill of activity in the monkey by analyzing the spatial and temporal activity of cells across the SC during the generation of visually guided saccades. 2. We recorded the activity of single cells while the monkey made saccades of different amplitudes (0.5-60 degrees). We recorded cells from locations extending from the rostral to caudal SC in order to sample cells whose optimal amplitudes ranged from small to large saccades. This allowed us to see any shift of activity across the SC before, during, and after saccades. It also allowed us to determine the fraction of the SC that was active during the successive phases of saccade generation. 3. During active visual fixation, the fixation cells in the rostral pole of the buildup layer showed an increased discharge rate. From the population reconstruction, we estimate that the zone of active cells spanned the most rostral 0.72 mm in each SC. Assuming the SC is 5 mm in length, approximately 15% of the cells lying along the horizontal meridian in the buildup layer would be active during fixation. 4. At least 100 ms before the initiation of a saccade, long-lead activity began to appear in the buildup layer at the site on the SC motor map related to the next saccade. Fixation activity in the rostral poles simultaneously began to diminish, but the cells in the burst layer remained relatively silent. 5. Approximately 25 ms before saccade onset, the fixation cells ceased firing and both burst and buildup cells began to burst. The active zone in the burst layer was estimated to be approximately 1.4 mm diam, occupying roughly 28% of the SC along a line running from the rostral pole through the center of the initially active zone. The size of this active area among the burst cells was independent of saccade amplitude.(ABSTRACT TRUNCATED AT 400 WORDS)


2009 ◽  
Vol 101 (6) ◽  
pp. 2934-2942 ◽  
Author(s):  
Rebecca A. Berman ◽  
Wilsaan M. Joiner ◽  
James Cavanaugh ◽  
Robert H. Wurtz

A cascade of neuronal signals precedes each saccadic eye movement to targets in the visual scene. In the cerebral cortex, this neuronal processing culminates in the frontal eye field (FEF), where neurons have bursts of activity before the saccade. This presaccadic activity is typically considered to drive downstream activity in the intermediate layers of the superior colliculus (SC), which receives direct projections from FEF. Consequently, the FEF activity is thought to be determined solely by earlier cortical processing and unaffected by activity in the SC. Recent evidence of an ascending path from the SC to FEF raises the possibility, however, that presaccadic activity in the FEF may also depend on input from the SC. Here we tested this possibility by recording from single FEF neurons during the reversible inactivation of SC. Our results indicate that presaccadic activity in the FEF does not require SC input: we never observed a significant reduction in FEF presaccadic activity when the SC was inactivated. Unexpectedly, in a third of experiments, SC inactivation elicited a significant increase in FEF presaccadic activity. The passive visual response of FEF neurons, in contrast, was virtually unaffected by inactivation of the SC. These findings show that presaccadic activity in the FEF does not originate in the SC but nevertheless may be influenced by modulatory signals ascending from the SC.


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