Effects of serotonin on retinotectal-, corticotectal-, and glutamate-induced activity in the superior colliculus of the hamster

1993 ◽  
Vol 70 (2) ◽  
pp. 723-732 ◽  
Author(s):  
X. Huang ◽  
R. D. Mooney ◽  
R. W. Rhoades

1. Single-unit recording and iontophoretic techniques were used to test the effects of serotonin (5-HT) on the responses of neurons in the superficial layers (the stratum griseum superficiale and stratum opticum) of the hamster's superior colliculus (SC). 2. Iontophoresis of 5-HT produced a visual response suppression of 40% or greater in 78.1% (n = 50) of 64 neurons tested. 5-HT did not augment the visual responses of any of the cells tested. The average response suppression was 75.3 +/- 21.2% (mean +/- S.D.). 3. Iontophoresis of 5-HT had significantly different effects on activation of SC cells by optic chiasm (OX) and visual cortical (CTX) stimulation. Application of 5-HT suppressed the OX-evoked responses of 96.9% (n = 31) of the 32 SC cells tested by at least 40%, and the average response suppression for all 32 neurons tested was 87.1 +/- 22.5%. Application of 5-HT suppressed the responses of only 35.7% (n = 10) of the 28 cells tested with CTX stimulation by at least 40%. The average response suppression for all 28 cells was 35.3 +/- 38.8%. 4. The effects of 5-HT on the glutamate-evoked responses of SC cells that were synaptically "isolated" by concurrent application of Mg2+ were also evaluated. Application of 5-HT produced a response suppression > or = 40% in 29.7% (n = 19) of the 64 neurons tested under these conditions. The average response suppression for all of the cells tested was 28.4 +/- 35.7%. This effect of 5-HT was significantly weaker than that on visually evoked responses of these neurons. 5. The present results demonstrate that 5-HT markedly depresses the visual responses of most superficial layer SC neurons. They suggest further that much of this effect is mediated by presynaptic inhibition of retinotectal transmission.

1996 ◽  
Vol 13 (2) ◽  
pp. 237-246 ◽  
Author(s):  
Yi Zhang ◽  
Richard D. ◽  
Carol A. Bennett-Clarke ◽  
Robert W. Rhoades

AbstractAutoradiography with 125I-neurotensin in normal and enucleated hamsters was used to define the distribution of receptors for this peptide in the superficial layers of the superior colliculus (SC). Neurotensin binding sites were densely distributed in the stratum griseum superficiale (SGS), and results from the enucleated animals indicated that they were not located on retinal axons. The effects of neurotensin on individual superficial layer cells were tested in single-unit recording experiments. Neurotensin was delivered via micropressure ejection during visual stimulation (n = 75 cells), or during electrical stimulation of either the optic chiasm (OX; n = 47 cells) or visual cortex (CTX; n = 29 cells). In comparison with control values, application of neurotensin decreased visual responses of all SC cells tested to 54.1 ± 34.9% (mean ± standard deviation; range of decrement 7.5 to 100%; nine cells showed no effect or an increase in visual activity, which for four of these was ≥30%). Neurotensin application also reduced responses to electrical stimulation of either OX or CTX, respectively, to 65.8 ± 36.5% of control values (range of decrement 2.6 to 97.4%; 12 neurons showed a weak increment ≤ 30%) and 68.0 ± 38.5% (range of decrement 3.3 to 100%; five cells showed no effect or an increment, in one case ≥ 30%). Of the 25 neurons tested with both OX and CTX stimulation, the correlation of evoked response suppression by neurotensin was highly significant (r = 0.70; P < 0.001). This suggests that the suppressive effects of neurotensin were common to both pathways. To test whether the inhibitory effects of neurotensin were presynaptic or postsynaptic, Mg2+ ions were ejected iontophoretically to abolish synaptic responses, and the neurons (n = 16) were activated by iontophoresis of glutamate and then tested with neurotensin. Neurotensin reduced the glutamate-evoked responses to an average 59.3 ± 37.9% of control values (range 2.3 to 92.5%; one cell showed an increment >30%). This result suggests that the site of action of neurotensin is most likely postsynaptic.


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.


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.


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.


Author(s):  
Stéphane Molotchnikoff ◽  
Michel Dubuc

SummaryThe responsiveness of the visual cortex (VC) and superior colliculus (SC) was simultaneously compared following conditioning “ON” or “OFF” stimulation, in the rabbit.Average evoked responses were recorded simultaneously from the visual cortex and superior colliculus. “ON” or “OFF” steps constituted the conditioning stimuli whereas the test stimulus consisted of optic nerve stimulation. All evoked responses exhibited a reversal of their polarity when the electrode was moved in the dorsoventral direction (Negative-Positive in the SC, Positive-Negative in the VC). This assured the somato-dentritic origin of the potentials. The results showed that responsiveness in both structures was significantly higher following an “OFF” stimulus than after an “ON” step. Collicular responsiveness was higher than in the VC when the same conditioning stimulus was applied. The spatial distribution of the source of “OFF” responses was circumscribed to the ventral part of the superficial layer of the superior colliculus. These results suggest specific properties associated with the brightening and dimming systems.


2005 ◽  
Vol 94 (4) ◽  
pp. 2491-2503 ◽  
Author(s):  
Keith A. Schneider ◽  
Sabine Kastner

The superior colliculus (SC) is a multimodal laminar structure located on the roof of the brain stem. The SC is a key structure in a distributed network of areas that mediate saccadic eye movements and shifts of attention across the visual field and has been extensively studied in nonhuman primates. In humans, it has proven difficult to study the SC with functional MRI (fMRI) because of its small size, deep location, and proximity to pulsating vascular structures. Here, we performed a series of high-resolution fMRI studies at 3 T to investigate basic visual response properties of the SC. The retinotopic organization of the SC was determined using the traveling wave method with flickering checkerboard stimuli presented at different polar angles and eccentricities. SC activations were confined to stimulation of the contralateral hemifield. Although a detailed retinotopic map was not observed, across subjects, the upper and lower visual fields were represented medially and laterally, respectively. Responses were dominantly evoked by stimuli presented along the horizontal meridian of the visual field. We also measured the sensitivity of the SC to luminance contrast, which has not been previously reported in primates. SC responses were nearly saturated by low contrast stimuli and showed only small response modulation with higher contrast stimuli, indicating high sensitivity to stimulus contrast. Responsiveness to stimulus motion in the SC was shown by robust activations evoked by moving versus static dot stimuli that could not be attributed to eye movements. The responses to contrast and motion stimuli were compared with those in the human lateral geniculate nucleus. Our results provide first insights into basic visual responses of the human SC and show the feasibility of studying subcortical structures using high-resolution fMRI.


2009 ◽  
Vol 101 (4) ◽  
pp. 1813-1822 ◽  
Author(s):  
P. S. Khayat ◽  
A. Pooresmaeili ◽  
P. R. Roelfsema

Neurons in the frontal eye fields (FEFs) register incoming visual information and select visual stimuli that are relevant for behavior. Here we investigated the timing of the visual response and the timing of selection by recording from single FEF neurons in a curve-tracing task that requires shifts of attention followed by an oculomotor response. We found that the behavioral selection signal in area FEF had a latency of 147 ms and that it was delayed substantially relative to the visual response, which occurred 50 ms after stimulus presentation. We compared the FEF responses to activity previously recorded in the primary visual cortex (area V1) during the same task. Visual responses in area V1 preceded the FEF responses, but the latencies of selection signals in areas V1 and FEF were similar. The similarity of timing of selection signals in structures at opposite ends of the visual cortical processing hierarchy supports the view that stimulus selection occurs in an interaction between widely separated cortical regions.


1995 ◽  
Vol 73 (5) ◽  
pp. 1988-2003 ◽  
Author(s):  
M. F. Walker ◽  
E. J. Fitzgibbon ◽  
M. E. Goldberg

1. Previous experiments have shown that visual neurons in the lateral intraparietal area (LIP) respond predictively to stimuli outside their classical receptive fields when an impending saccade will bring those stimuli into their receptive fields. Because LIP projects strongly to the intermediate layers of the superior colliculus, we sought to demonstrate similar predictive responses in the monkey colliculus. 2. We studied the behavior of 90 visually responsive neurons in the superficial and intermediate layers of the superior colliculus of two rhesus monkeys (Macaca mulatta) when visual stimuli or the locations of remembered stimuli were brought into their receptive fields by a saccade. 3. Thirty percent (18/60) of intermediate layer visuomovement cells responded predictively before a saccade outside the movement field of the neuron when that saccade would bring the location of a stimulus into the receptive field. Each of these neurons did not respond to the stimulus unless an eye movement brought it into its receptive field, nor did it discharge in association with the eye movement unless it brought a stimulus into its receptive field. 4. These neurons were located in the deeper parts of the intermediate layers and had relatively larger receptive fields and movement fields than the cells at the top of the intermediate layers. 5. The predictive responses of most of these neurons (16/18, 89%) did not require that the stimulus be relevant to the monkey's rewarded behavior. However, for some neurons the predictive response was enhanced when the stimulus was the target of a subsequent saccade into the neuron's movement field. 6. Most neurons with predictive responses responded with a similar magnitude and latency to a continuous stimulus that remained on after the saccade, and to the same stimulus when it was only flashed for 50 ms coincident with the onset of the saccade target and thus never appeared within the cell's classical receptive field. 7. The visual response of neurons in the intermediate layers of the colliculus is suppressed during the saccade itself. Neurons that showed predictive responses began to discharge before the saccade, were suppressed during the saccade, and usually resumed discharging after the saccade. 8. Three neurons in the intermediate layers responded tonically from stimulus appearance to saccade without a presaccadic burst. These neurons responded predictively to a stimulus that was going to be the target for a second saccade, but not to an irrelevant flashed stimulus. 9. No superficial layer neuron (0/27) responded predictively when a stimulus would not be brought into their receptive fields by a saccade.(ABSTRACT TRUNCATED AT 400 WORDS)


1988 ◽  
Vol 59 (6) ◽  
pp. 1783-1797 ◽  
Author(s):  
C. L. Colby

1. The dorsal lateral geniculate nucleus (LGN) of the cat is a major thalamic relay between the retina and several visual cortical areas. These cortical areas in turn project to the superior colliculus (SC). The aim of the present experiment was to determine which LGN layers provide a necessary input to the corticotectal circuit. 2. Individual layers of the LGN were reversibly inactivated by microinjection of cobalt chloride during recording of visual responses in the retinotopically corresponding part of the superior colliculus. 3. For cells driven through the contralateral eye, inactivation of layer A or the medial interlaminar nucleus (MIN) had little effect on visual responsiveness in the superior colliculus. In contrast, inactivation of layer C abolished visual responses at one-quarter of the SC recording sites, reduced responses at another quarter, and left half of the recording sites unaffected. 4. For cells driven through the ipsilateral eye, inactivation of layer C1 or the MIN had no effect. Inactivation of layer A1 uniformly reduced visual responses in the superior colliculus and usually abolished them entirely. 5. These results are compatible with previous work showing that cortical input to the SC originates from Y-cells. They indicate that two of the five Y-cell containing layers (A1 and C) provide major inputs to the corticotectal circuit. The results suggest that layer A1 is functionally allied to layer C as well as to layer A.


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