scholarly journals Dissociation of visual and saccade-related responses in superior colliculus neurons

1980 ◽  
Vol 43 (1) ◽  
pp. 207-232 ◽  
Author(s):  
L. E. Mays ◽  
D. L. Sparks

1. Single-unit activity was recorded from the superior colliculus (SC) of monkeys trained to look to visual targets presented on an oscilloscope screen. On one task, target localization required that information concerning the retinal position of the target be combined with information concerning current or future eye position. This task also permitted a dissociation between the site of retinal stimulation and the metrics of the saccade triggered by the stimulation. 2. Vigorous visual responses of superficial SC neurons may occur that do not result in the activation of underlying saccade-related cells. The activity of these neurons signals the occurrence of a visual stimulus, whether or not the stimulus is selected for foveal viewing. 3. Saccade-related (SR) discharges of most intermediate and deep-layer SC neurons precede saccades with particular vectors, regardless of the region of retinal activation initiating the saccade. The discharge of these neurons is tightly coupled to saccade onset, even if changes in eye position have occurred since target appearance. Thus, the discharge of these SR neurons must occur after retinal error and eye-position signals have been combined to compute the necessary saccade vector. For most SR neurons, direct retinal activation of overlying visual neurons had no effect on either the vigor or probability of a SR discharge. The discharge of overlying visual cells is neither necessary nor sufficient to activate most SR cells. 4. The discharge of some SR cells is dependent on prior activation of overlying visual cells. Of 53 SR cells, only 3 were completely dependent on visual stimulation, while another 8 discharged less vigorously if corresponding visual activation failed to occur. 5. About one-quarter of the SR cells showed long-lead preburst activity. This activation was characterized by a low level of firing, which began after the saccade signal and continued until a saccade-linked burst occurred. 6. Cells were isolated that were visually responsive yet discharged prior to saccades in the absence of appropriate retinal stimulation. No component of the discharge of these quasi-visual (QV) cells appeared to be motor in the usual sense. The activity of these neurons appears to reflect eye-position error (the difference between actual and desired eye position) and to hold this information in spatial register until a saccade occurs or is cancelled. 7. It is concluded that the presumed linkage, implied in earlier versions of the foveation hypothesis, between the superficial layers (receiving direct retinal inputs) and the deeper layers of the SC is not necessary for the activation of SR neurons. Results suggest that the SC must generate or receive a signal that combines retinal error and eye-position information. These findings are discussed in terms of current models of the saccadic-control system.

1993 ◽  
Vol 70 (2) ◽  
pp. 559-575 ◽  
Author(s):  
D. P. Munoz ◽  
R. H. Wurtz

1. We studied the role of the superior colliculus (SC) in the control of visual fixation by recording from cells in the rostral pole of the SC in awake monkeys that were trained to perform fixation and saccade tasks. 2. We identified a subset of neurons in three monkeys that we refer to as fixation cells. These cells increased their tonic discharge rate when the monkey actively fixated a visible target spot to obtain a reward. This sustained activity persisted when the visual stimulation of the target spot was momentarily removed but the monkey was required to continue fixation. 3. The fixation cells were in the rostral pole of the SC. As the electrode descended through the SC, we encountered visual cells with foveal and parafoveal receptive fields most superficially, saccade-related burst cells with parafoveal movement fields below these visual cells, and fixation cells below the burst cells. From this sequence in depth, the fixation cells appeared to be centered in the deeper reaches of the intermediate layers, and this was confirmed by small marking lesions identified histologically. 4. During saccades, the tonically active fixation cells showed a pause in their rate of discharge. The duration of this pause was correlated to the duration of the saccade. Many cells did not decrease their discharge rate for small-amplitude contraversive saccades. 5. The saccade-related pause in fixation cell discharge always began before the onset of the saccade. The mean time from pause onset to saccade onset for contraversive saccades and ipsiversive saccades was 36.2 and 33.0 ms, respectively. Most fixation cells were reactivated before the end of contraversive saccades. The mean time from saccade terminatioN to pause end was -2.6 ms for contraversive saccades and 9.9 ms for ipsiversive saccades. The end of the saccade-related pause in fixation cell discharge was more tightly correlated to saccade termination, than pause onset was to saccade onset. 6. After the saccade-related pause in discharge, many fixation cells showed an increased discharge rate exceeding that before the pause. This increased postsaccadic discharge rate persisted for several hundred milliseconds. 7. The discharge rate of fixation cells was not consistently altered when the monkey actively fixated targets requiring different orbital positions. 8. Fixation cells discharged during smooth pursuit eye movements as they did during fixation. They maintained a steady tonic discharge during pursuit at different speeds and in different directions, provided the monkey looked at the moving target.(ABSTRACT TRUNCATED AT 400 WORDS)


1991 ◽  
Vol 66 (2) ◽  
pp. 485-496 ◽  
Author(s):  
D. L. Robinson ◽  
J. W. McClurkin ◽  
C. Kertzman ◽  
S. E. Petersen

1. We recorded from single neurons in awake, trained rhesus monkeys in a lighted environment and compared responses to stimulus movement during periods of fixation with those to motion caused by saccadic or pursuit eye movements. Neurons in the inferior pulvinar (PI), lateral pulvinar (PL), and superior colliculus were tested. 2. Cells in PI and PL respond to stimulus movement over a wide range of speeds. Some of these cells do not respond to comparable stimulus motion, or discharge only weakly, when it is generated by saccadic or pursuit eye movements. Other neurons respond equivalently to both types of motion. Cells in the superficial layers of the superior colliculus have similar properties to those in PI and PL. 3. When tested in the dark to reduce visual stimulation from the background, cells in PI and PL still do not respond to motion generated by eye movements. Some of these cells have a suppression of activity after saccadic eye movements made in total darkness. These data suggest that an extraretinal signal suppresses responses to visual stimuli during eye movements. 4. The suppression of responses to stimuli during eye movements is not an absolute effect. Images brighter than 2.0 log units above background illumination evoke responses from cells in PI and PL. The suppression appears stronger in the superior colliculus than in PI and PL. 5. These experiments demonstrate that many cells in PI and PL have a suppression of their responses to stimuli that cross their receptive fields during eye movements. These cells are probably suppressed by an extraretinal signal. Comparable effects are present in the superficial layers of the superior colliculus. These properties in PI and PL may reflect the function of the ascending tectopulvinar system.


2000 ◽  
Vol 17 (2) ◽  
pp. 283-289 ◽  
Author(s):  
K.E. BINNS ◽  
T.E. SALT

In the rat, the superficial gray layer (SGS) of the superior colliculus receives glutamatergic projections from the contralateral retina and from the visual cortex. A few fibers from the ipsilateral retina also directly innervate the SGS, but most of the ipsilateral visual input is provided by cholinergic afferents from the opposing parabigeminal nucleus (PBG). Thus, visual input carried by cholinergic afferents may have a functional influence on the responses of SGS neurones. When single neuronal extracellular recording and iontophoretic drug application were employed to examine this possibility, cholinergic agonists were found to depress responses to visual stimulation. Lobeline and 1-acetyl-4-methylpiperazine both depressed visually evoked activity and had a tendency to reduce the background firing rate of the neurones. Carbachol depressed the visual responses without any significant effect on the ongoing activity, while the muscarinic receptor selective agonist methacholine increased the background activity of the neurones and reduced their visual responses. Lobeline was chosen for further studies on the role of nicotinic receptors in SGS. Given that nicotinic receptors are associated with retinal terminals in SGS, and that the activation of presynaptic nicotinic receptors normally facilitates transmitter release (in this case glutamate release), the depressant effects of nicotinic agonists are intriguing. However, many retinal afferents contact inhibitory neurones in SGS; thus it is possible that the increase in glutamate release in turn facilitates the liberation of GABA which goes on to inhibit the visual responses. We therefore attempted to reverse the effects of lobeline with GABA receptor antagonists. The depressant effects of lobeline on the visual response could not be reversed by the GABAA antagonist bicuculline, but the GABAB antagonist CGP 35348 reduced the effects of lobeline. We hypothesize that cholinergic drive from the parabigeminal nucleus may activate presynaptic nicotinic receptors on retinal terminals, thereby facilitating the release of glutamate onto inhibitory neurones. Consequently GABA is released, activating GABAB receptors, and thus the ultimate effect of nicotinic receptor activation is to depress visual responses.


1979 ◽  
Vol 42 (1) ◽  
pp. 1-15 ◽  
Author(s):  
G. Mower ◽  
A. Gibson ◽  
M. Glickstein

1. The superior colliculus projects to the dorsolateral nucleus of the pons. Retrograde transport of horseradish peroxidase (HRP) revealed that cells in the superior colliculus, which send their axons to the pons, lie in both superficial (III) and deep (IV--VII) layers. Superficial cells outnumbered deep cells. The inferior colliculus also projects heavily to the dorsolateral pontine nucleus. 2. Dorsolateral pontine visual cells were activated only by visual stimulation. Cells responsive to somatic or auditory stimulation were also found in the dorsolateral nucleus, and they too responded to only one sense modality. 3. Of the dorsolateral pontine visual cells, 69% were directionally selective. 4. Dorsolateral pontine visual cells were responsive to moving targets over a wide range of stimulus velocities. Velocities between 25 and 100 degrees/s were the most effective. No cells responded to a stationary stimulus. 5. Single-spot targets were the most effective stimuli. Stimulus size was a more important parameter than stimulus configuration. Many cells had inhibitory regions outside of their excitatory fields. 6. The excitatory receptive fields of dorsolateral pontine cells were very large (median, 1,100 deg2). 7. Nearly all receptive fields were centered in the contralateral visual hemifield, and 91% of the dorsolateral visual cells were activated from either eye. 8. We conclude that the visual cells in the dorsolateral nucleus have receptive-field properties that are similar to those of cells in the superior colliculus. The preference of dorsolateral cells for single-spot targets contrasts strongly with the multiple-spot preference of medial pontine cells, which receive their input from visual cortex.


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)


1994 ◽  
Vol 11 (6) ◽  
pp. 1163-1173 ◽  
Author(s):  
Richard D. Mooney ◽  
Yi Zhang ◽  
Robert W. Rhoades

AbstractSuperficial layer superior colliculus (SC) neurons were recorded extracellularly with multibarreled recording/ejecting micropipettes. Angiotensin II was delivered via micropressure ejection during visual stimulation (n = 215 cells), or during electrical stimulation of either the optic chiasm (OX; n = 150 cells) or visual cortex (CTX; n = 42 cells). Application of angiotensin II decreased visual responses of SC cells to 43.8% ± 30.7% (mean ± S.D.) and reduced responses to electrical stimulation of the OX and CTX to 58.6% ± 34.1% and 43.8% ± 30.7% of control values, respectively. Angiotensin II enhanced responses by at least 30% in only 6 cells (1.5%). Of the 35 neurons tested with both OX and CTX stimulation, the correlation of evoked response suppression by angiotensin II was highly significant (r = 0.69; P < 0.001). This suggests that the suppressive effects of angiotensin II were common to both pathways. To test whether the inhibitory effects of angiotensin II were presynaptic or postsynaptic, Mg2+ ions were ejected iontophoretically to abolish synaptic responses, and the neurons were activated by iontophoresis of glutamate and then tested with angiotensin II. Angiotensin II reduced the glutamate-evoked responses to an average 29.1% ± 21.1% of control values (n = 9 cells). This suggests that the site of action of angiotensin II is most likely postsynaptic. To identify which receptors were involved in these effects, angiotensin II was ejected concurrently with the AT1 antagonist Losartan (DUP753) or with either of two AT2 antagonists, CGP42112A or PD123177. Losartan antagonized the action of angiotensin II in 65.6% of the cells tested (n = 99) and CGP42112A and PD123177 had antagonistic effects in 58% (n = 65) and 60% (n = 5), respectively. Both classes of antagonists were tested in 29 cells; and there was no significant correlation between their effectiveness. These results suggest that both AT1, and AT2 receptors may independently mediate the suppressive effects of angiotensin II, and that collicular neurons may have either or both receptor subtypes.


1995 ◽  
Vol 12 (3) ◽  
pp. 563-571 ◽  
Author(s):  
K.E. Binns ◽  
T.E. Salt

AbstractIn visual neurones of the superficial layers of the superior colliculus (SSC), repetitive stimulation causes a progressive decline in the size of the response to the stimulus, usually known as response habituation or response adaptation. A mechanism has been proposed in which habituation results from coactivation of excitatory and inhibitory neurones, and the responses of the inhibitory neurones block the response to subsequent stimulus presentations. Excitatory amino acid (EAA) neurotransmitters mediate visual responses via NMDA and non-NMDA receptors in cat SSC. We have investigated the role of these receptors in the generation of response habituation. Following the iontophoretic application of the EAA antagonists CNQX, APS or CPP, repetitive visual stimulation paradigms which normally produce response habituation no longer do so. Indeed the response to each presentation of the stimulus is similar. Intravenous administration of the dissociative anesthetic ketamine (2–10 mg/kg) had similar actions to iontophoretically applied NMDA antagonists. The data imply that intracollicular mechanisms activated by NMDA and non-NMDA receptors contribute to the generation of the inhibitory responses in SCC which lead to response habituation. Furthermore, the effects seen with ketamine anesthesia suggest that the use of ketamine in studies of sensory systems may result in the lack of habituation.


1999 ◽  
Vol 16 (3) ◽  
pp. 541-555 ◽  
Author(s):  
YI ZHANG ◽  
RICHARD D. MOONEY ◽  
ROBERT W. RHOADES

Single-unit recording and micropressure ejection techniques were used to test the effects of norepinephrine (NE) on the responses of neurons in the superficial layers (the stratum griseum superficiale and stratum opticum) of the hamster's superior colliculus (SC). Application of NE suppressed visually evoked responses by ≥30% in 75% of 40 neurons tested and produced ≥30% augmentation of responses in only 5%. The decrement in response strength was mimicked by application of the α2 adrenoceptor agonist, p-aminoclonidine, the nonspecific β agonist, isoproterenol, and the β1 agonist, dobutamine. These agents had similar effects on responses evoked by electrical stimulation of the optic chiasm and visual cortex. The α1 agonist, methoxamine, augmented the light-evoked responses of 53% of 49 SC cells by ≥30%, but had little effect on responses evoked by electrical stimulation of optic chiasm or visual cortex. The effects of adrenergic agonists upon the glutamate-evoked responses of SC cells that were synaptically “isolated” by concurrent application of Mg2+ were similar to those obtained during visual stimulation. Analysis of effects of NE on visually evoked and background activity indicated that application of this amine did not significantly enhance signal-to-noise ratios for most superficial layer SC neurons, and signal-to-noise ratios were in some cases reduced. These results indicate that NE acts primarily through α2 and β1 receptors to suppress the visual responses of SC neurons. Activation of either of these receptors reduces the responses of SC neurons to either of their two major visual inputs as well as to direct stimulation by glutamate, and it would thus appear that these effects are primarily postsynaptic.


1995 ◽  
Vol 73 (6) ◽  
pp. 2507-2521 ◽  
Author(s):  
T. X. Fan ◽  
A. E. Weber ◽  
G. E. Pickard ◽  
K. M. Faber ◽  
M. Ariel

1. Using an isolated turtle brain preparation, we made extracellular spike recordings in the dorsal midbrain during visual stimulation. Single units were isolated by their response to a slow-moving full-field visual pattern imaged on the contralateral retina. This stimulus elicits responses from the basal optic nucleus (BON) and the cerebellar cortex using a similar preparation. Direction and speed tuning were then analyzed, as well as the size and position of the receptive field. 2. In one brain stem region, anterior to the optic tectum and deep to the dorsal surface, all of the visually responsive neurons were direction sensitive (DS) to contralateral retinal stimulation. The location and properties of these cells indicate that they are in the mesencephalic lentiform nucleus (nLM). Anterograde transport of intravitreally injected horseradish peroxidase revealed that this pretectal nucleus receives direct input from the contralateral eye. 3. All but 2 of the 48 cells of the nLM were strongly DS. The most effective stimulus was a slowly moving complex visual pattern that drifted nasally in the contralateral visual field. Brief flashes of spots, patterns, or diffuse light were much less effective. Receptive fields were large and usually (9 of 13 cells) centered in the superior visual field near the horizon and nasal to the blind spot. 4. The visual responses of nLM cells were compared to those of cells in the superficial layers of the optic tectum. In contrast to nLM, the responses of tectal cells were heterogeneous and frequently not DS. Neither tectum or nLM cells had much spontaneous spike activity during darkness or stationary patterns. On the other hand, visual responses of nLM cells were very similar to those of the BON, where neurons also had low spontaneous activity, preferred slow-moving patterns, and were DS. However, nLM and BON exhibit different distributions of preferred directions. Most nLM cells preferred temporal-to-nasal motion, whereas BON cells preferred almost any direction, although few preferred the nasal direction. nLM cell responses were not affected by removal of the ventral brain stem including the BON. 5. The visual properties of nLM cells recorded in vitro were very similar to those that were recorded in intact turtles.(ABSTRACT TRUNCATED AT 400 WORDS)


1978 ◽  
Vol 41 (1) ◽  
pp. 55-64 ◽  
Author(s):  
B. E. Stein

1. The effects of cortical cooling on the responses of cells to visual, somatic, and acoustic stimuli were studied in the cat superior colliculus (SC). When the visual cortex was cooled, the responses of many visual cells of the SC were depressed or eliminated, but the activity of nonvisual cells remained unchanged. This response depression was found in visual cells located in both superficial and deep laminae and was most pronounced in neurons which were binocular and directionally selective. 2. Cooling somatic and/or auditory cortex had no effect on visual SC cells and, with few exceptions, did not alter the activity of somatic or acoustic cells either. 3. The specificity of visual cortex influences on visual responding in the SC was most apparent in multimodal cells. In trimodal cells, the simultaneous cooling of visual, somatic, and auditory cortex eliminated responses to visual stimuli, but did not affect responses to somatic or acoustic stimuli. Visual responses were returned to the precooling level in both unimodal and multimodal cells by cortical rewarming. 4. The present experiments indicate that despite the organizational parallels among visual, somatic, and acoustic cells of the cat SC, the influences they receive from cortex are non-equivalent. Cortical influences appear to play a more critical role in the responses of visual cells than in the responses of somatic and acoustic cells. These observations raise questions about the functional significance of nonvisual corticotectal systems.


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