Tectorecipient zone of cat lateral posterior nucleus: evidence that collicular afferents contain acetylcholinesterase

Summary The superficial layers of the cat's superior colliculus innervate the medial subdivision of the thalamic lateral posterior nucleus (LPm). LPm is set off from adjoining thalamic zones by its denser staining for acetylcholinesterase (AChE). We sought to learn whether the tectal afferents to LPm might themselves be the source of the enzyme staining by examining the effects of collicular lesions on the thalamic staining pattern. Large excitotoxin lesions of the colliculus largely eliminated AChE staining in the ipsilateral LPm. By contrast, fibersparing lesions of LPm itself left AChE staining nearly unchanged. Destruction of collicular neurons by excitotoxins dramatically reduced AChE staining in fibers of the brachium and superficial gray layer of the superior colliculus. The reduction was especially pronounced in the lower part of the superficial gray layer, in which LP-projecting collicular neurons are located. These results are consistent with the view that LP-projecting collicular neurons synthesize AChE and account for much of the histochemically detectable enzyme present both in the lower superficial gray layer and in LPm. In the colliculus, the excitotoxin lesions spared AChE staining in a thin sheet at the upper border of the superficial gray layer and in the enzyme-positive patches in the intermediate layers. This surviving tectal AChE thus is probably presynaptic and could be contained at least partly in cholinergic afferents from the parabigeminal nucleus and pontomesencephalic tegmentum. The collicular lesions had no obvious effect on AChE staining in the parabigeminal nucleus or in the C-laminae or ventral division of the lateral geniculate nucleus.     

Relation of the parabigeminal nucleus to the superior colliculus and dorsal lateral geniculate nucleus in the hooded rat

Summary The retino-recipient layers of the superior colliculus project predominantly to the dorsal and ventral divisions of the ipsilateral parabigeminal nucleus, while receiving an input chiefly from the medial division of the contralateral nucleus. A variety of retrograde tracing techniques was used to confirm that there is a projection from the medial division of the parabigeminal nucleus to the contralateral dorsal lateral geniculate nucleus in normal adult hooded rats. Some parabigeminal cells branch to supply both dorsal lateral geniculate nucleus and retino-recipient layers of the superior colliculus.     

Modulations of the lateral geniculate nucleus cell responses by a second discrete conditioning stimulus: implications of the superior colliculus in rabbits

Summary This study analyzes the interactions between two discrete stimuli located in the visual field of the rabbit at the lateral geniculate level. Single unit recordings were carried out simultaneously from the superior colliculus (SC) and lateral geniculate nucleus (LGN) in anesthetized and paralyzed rabbits. A first conditioning stimulus (most often a moving target) was positioned in the receptive field of the collicular cell to ensure activation of the retino-collicular path. A second test stimulus was introduced into the receptive field of the LGN cell. The presentation of this latter stimulus was timed so as to fire the geniculate cell at various delays after the collicular neuron had responded to its own stimulus. The spontaneous firing of each cell was unaffected by the stimulus appropriate to the complementary unit. The conditioning collicular stimulus produced increases or decreases in geniculate responses. This modulation may eventually reduce the direction specificity of a geniculate unit. The fluctuations of the geniculate responses peaked 200 to 300 ms after collicular cells had responded. In a separate series of experiments the influence of the conditioning stimulus on geniculate responses was abolished when the SC was locally inactivated. These results suggest that the well documented colliculo-geniculate system mediates the interactions of several stimuli in the visual field. The outcome of this processing results in a modulation of geniculate responses.     

The projection from the superior colliculus to the lateral reticular nucleus in the cat as studied with retrograde transport of WGA-HRP

Summary Medium-sized and large superior collicular neurons were retrogradely labelled after small ejections of the wheat germ agglutinin-horseradish peroxidase complex in the lateral reticular nucleus of the feline medulla. The projection from the superior colliculus to the lateral reticular nucleus is bilateral with a contralateral predominance. It originates mainly from the intermediate, but also from the deep gray layer of the superior colliculus. Our observations provide evidence that the lateral reticular nucleus is an important target of tectal efferents. The findings are discussed in relation to the organization of other fiber connections of the superior colliculus.     

Control of recurrent inhibition of the lateral geniculate nucleus by afferents from the superior colliculus of the rabbit: a possible mechanism of saccadic suppression

Summary Stimulation of the ipsilateral superior colliculus elicited a short burst of discharges of the recurrent inhibitory interneurones in the geniculocortical pathway of the rabbit. The most effective stimulating sites for this excitation were located in the deep layers rather than the superficial layers of the superior colliculus. The short latency of the response (2.3±0.6 ms) implied an oligo-synaptic excitatory pathway from the deep layers of the superior colliculus to the recurrent interneurones located in the caudal reticular nucleus of the thalamus. Following the excitation of the inter-neurone, there was a prolonged inhibition which started 10–30 ms and ended 150 ms after the collicular stimulation. The maximal inhibition occurred 50–70 ms after the stimulation. The effects of collicular stimulation on the recurrent inhibitory interneurones may be concerned with the inhibition of the visual pathway during saccades and with the disinhibition of facilitation during fixation of a new visual target.     

Response properties of neurons in area 17 projecting to the striate-recipient zone of the cat's lateralis posterior-pulvinar complex: comparison with cortico-tectal cells

The main input of the lateral part of the cat's lateralis posterior-pulvinar complex (LP-P) comes from the primary visual cortex. We investigated the response properties of cells in area 17 projecting to the striate-recipient zone (LPl) of the cat's LP-P complex. The cells' receptive fields were stimulated with drifting sine-wave gratings. Cells whose fibres terminate in the superior colliculus were also recorded, to determine how their properties compare with those of cortico-LPl cells and to investigate the possibility that LPl is innervated by collaterals of cortico-tectal units. A total of 26 cells in the striate cortex were identified by antidromic activation from the LPl (mean latency 2.2 ms) and 22 from the colliculus (mean latency 2.5 ms). Only six cortical cells could be activated from the LPl and the colliculus. All cortico-LPl cells except for two responded to drifting sinusoidal gratings with unmodulated discharges (AC/DC ratios <1). On the basis of their modulation index, these units were classified as complex cells. All cortico-LPl cells were selective for the orientation of gratings (mean bandwidth of 28°). There was a tendency for cortico-LPl cells to prefer vertical and horizontal orientations. More than half of these cells (57%) were direction selective. Strong orientation anisotropies were also found in the receptive fields of cortico-tectal cells, since almost all units responded preferentially to horizontally oriented gratings. The mean preferred spatial and temporal frequencies of cortico-LPl cells were 0.74 c/deg (bandwidth 2.03 octaves) and 2.7 Hz (bandwidth 2.5 octaves), respectively. These properties did not differ significantly from those of cortico-tectal cells. Most cortico-LPl cells (72%) exhibited contrast-response curves with saturation at low contrast (mean half-saturation 0.2). For the remaining units, the responses increased linearly with contrast without clear saturation. For more than half of cortico-tectal cells (60%), the contrast function was also characterised by a response saturation. Almost all cortico-LPl cells responded to moving random dot patterns with mean tuning functions of 43.6°. Standard as well as special complex cells were found to be equally responsive to the motion of visual noise. Similar properties were recorded for cortico-tectal cells (mean bandwidth of 44.2°). Cortico-LPl and cortico-tectal cells were either binocularly or monocularly driven by the contralateral eye and their mean spontaneous firing rates were 11.7 and 10.9 spikes/s, respectively. These cells were presumably located in layer V. Stimulation of LPl and colliculus also evoked trans-synaptic responses in area 17. The average latency of the orthodromic responses from LPl was much shorter than that from the colliculus (medians 3.5 and 50 ms, respectively). The findings indicate that almost all cortico-LPl units have complex receptive fields and that their overall properties differ from those of recipient cells in LPl. These results also indicate that LPl is not likely to be innervated by collaterals of fibres of cortico-tectal cells. While cortico-LPl and cortico-tectal cells appear to form two distinct populations, there is no significant difference between the overall properties of these two cell groups.     

Comparison of the effects of superior colliculus and pulvinar lesions on visual search and tachistoscopic pattern discrimination in monkeys

Summary In order to investigate whether pulvinar lesions produce behavioral impairments similar to those that follow superior colliculus lesions, monkeys were tested on a visual search task before and after receiving radiofrequency lesions of either the superior colliculus or pulvinar. The animals searched for a small target pattern within an array of varying numbers of irrelevant patterns. After receiving colliculus lesions, the animals showed marked postoperative increases in either search time, percent errors, or both. By contrast, pulvinar lesions had little or no effect on visual search performance. Similarly, in learning to search for a target they had not previously seen, animals with colliculus lesions were impaired relative to unoperated controls, whereas pulvinar-lesioned animals did not differ from controls. In an attempt to confirm the finding that pulvinar lesions impair tachistoscopic pattern discrimination, we determined exposure-duration thresholds of pulvinar- and colliculus-lesioned monkeys for performance of a pattern discrimination. The thresholds of the colliculus-lesioned monkeys were elevated 20-fold relative to controls. By contrast, thresholds of the pulvinar-lesioned monkeys were normal. We conclude that the pulvinar is not critical for the attentional processes in which the superior colliculus participates.     

Evidence of a collicular input to the dorsal lateral geniculate nucleus in rabbits — electrophysiology

Summary In anesthetized and paralyzed rabbits, unit responses of lateral geniculate nucleus (LGN) cells to focal electrical stimulation of the superior colliculus were studied. Geniculate responses to collicular stimulation (SCS) were compared with responses to optic nerve shock (ONS). A weak correlation coefficient suggested that collicular stimulation did not fire geniculate cells through collateral activation. Further differentiation between collicular and retinofugal inputs to LGN was made possible by repetitive stimulation. Geniculate cells which responded to collicular stimulation were relay cells as they were antidromically invaded from the visual cortex. This ruled out recordings from the ventral geniculate, since this area does not project to the visual cortex. A direct colliculo-geniculate pathway was revealed by antidromic activation of collicular cells by stimulation of the dorsal LGN. Finally, triggering flashes by collicular firing resulted in a marked modification of the geniculate test response. The results suggest that the superior colliculus sends fibers to the LGN and is capable of modulating the retino-cortical neuronal message at the level of the LGN.     

Differential expression of vesicular glutamate transporters 1 and 2 may identify distinct modes of glutamatergic transmission in the macaque visual system

Glutamate is the primary neurotransmitter utilized by the mammalian visual system for excitatory neurotransmission. The sequestration of glutamate into synaptic vesicles, and the subsequent transport of filled vesicles to the presynaptic terminal membrane, is regulated by a family of proteins known as vesicular glutamate transporters (VGLUTs). Two VGLUT proteins, VGLUT1 and VGLUT2, characterize distinct sets of glutamatergic projections between visual structures in rodents and prosimian primates, yet little is known about their distributions in the visual system of anthropoid primates. We have examined the mRNA and protein expression patterns of VGLUT1 and VGLUT2 in the visual system of macaque monkeys, an Old World anthropoid primate, in order to determine their relative distributions in the superior colliculus, lateral geniculate nucleus, pulvinar complex, V1 and V2. Distinct expression patterns for both VGLUT1 and VGLUT2 identified architectonic boundaries in all structures, as well as anatomical subdivisions of the superior colliculus, pulvinar complex, and V1. These results suggest that VGLUT1 and VGLUT2 clearly identify regions of glutamatergic input in visual structures, and may identify common architectonic features of visual areas and nuclei across the primate radiation. Additionally, we find that VGLUT1 and VGLUT2 characterize distinct subsets of glutamatergic projections in the macaque visual system; VGLUT2 predominates in driving or feedforward projections from lower order to higher order visual structures while VGLUT1 predominates in modulatory or feedback projections from higher order to lower order visual structures. The distribution of these two proteins suggests that VGLUT1 and VGLUT2 may identify class 1 and class 2 type glutamatergic projections within the primate visual system (Sherman and Guillery, 2006).     

Cortico-tectal and intertectal modulation of visual responses in the rat's superior colliculus

Summary In rats under urethane anesthesia, electrolytic destruction of one superior colliculus resulted in an increase in the amplitude of the light-evoked potential recorded in the remaining contralateral superior colliculus. In another group of rats, unilateral ablation of visual cortex produced a depression of the light-evoked potential recorded in the ipsilateral superior colliculus. However, in these same animals, subsequent destruction of the contralateral superior colliculus resulted in an increase in the amplitude of the tectal response to near normal levels. These findings suggest that the activity of the colliculus of the rat is subject to two opposing and tonic influences: 1. cortico-tectal facilitation, and 2. tectotectal inhibition.This study was supported by a grant from the National Research Council of Canada to Dr. A. Monjan. I would like to thank Dr. Monjan for his guidance and assistance in this work.     

Bilateral impact of unilateral visual cortex lesions on the superior colliculus

We examined the functional impact of a long-standing, unilateral primary visual cortex lesion on the superior colliculus (SC) using radiolabeled 2-deoxyglucose (2DG) as a marker of neural activity. In accord with known corticotectal connectivity and functional influence, 2DG uptake in the superficial layers of the ipsilesional SC was decreased. We also found a decrease in the superficial layers of the contralesional SC. These data suggest that modifications in activity in one SC can have a substantial influence on activity in its contralateral partner, and that processing in one visual hemifield does not occur independently of processing of signals in the opposite hemifield. The effects are not mediated by the contralateral hemisphere but are probably mediated by intercollicular circuitry.     

Receptive fields of single cells in the cat's superior colliculus

Summary Receptive field analysis of single units in the superior colliculus of the mid-pontine, pretrigeminal cat has confirmed previous reports of directionally selective units in the tectum. The directional property was based principally upon a unilateral inhibitory mechanism, although some directional responses to small moving objects depended equally upon summation of excitation. Receptive field size varied greatly, with field diameters not uncommonly exceeding 30 degrees. Fields near the area centralis and along the horizontal meridian tended to be smaller than those elsewhere. An inhibitory influence from the field periphery was demonstrated.Post-doctoral fellow of the National Science Foundation. Present address: Department of Experimental Psychology, Walter Reed Army Institute of Research, Washington, D. C. 20012 (USA).     

Effects of unilateral superior colliculus ablation on oculomotor and vestibulo-ocular responses in the cat

Summary 1. Unilateral lesions of the superior colliculus were made in normal cats. Following the operation, animals exhibited a typical neglect for contralateral visual space and forced circling toward the ipsilateral side. Optokinetic nystagmus was decreased for a stimulus moving toward the ipsilateral side, particularly in the temporal-to-nasal direction when the eye contralateral to the lesion was stimulated alone. — 2. When tested in the dark, animals exhibited a strong imbalance of their vestibulo-ocular responses (VOR) to velocity steps or to sinusoidal oscillations. Rotation of the animal toward the ipsilateral side produced a VOR with a higher gain, and a shorter phase-lead than in pre-operative controls. VOR was decreased in the opposite direction to a smaller extent, however. The overall asymmetry between the two sides at the post-operative stage was about 40%. — 3. In two animals, spontaneous nystagmus was present in the dark with the fast phase toward the ipsilateral side. — 4. Visual suppression of VOR was abolished during ipsiversive rotation and was still present during contraversive rotation. — 5. The effects of unilateral colliculectomy on VOR were transient. Spontaneous nystagmus disappeared in 3 days. VOR asymmetry in the dark was no longer present after 2–3 weeks. Loss of visual VOR suppression persisted for a few more days. — 6. Superior colliculus exerts a tonic control on static and dynamic components of VOR. This control may mediate part of VOR visual modulation and provide a substitutive input for compensation of pathological VOR asymmetry.     

The superior colliculus neurons which project to the dorsal and ventral lateral geniculate nuclei in the cat

Summary Cells in the cat superior colliculus which project to the ventral and dorsal lateral geniculate nuclei (VLG and DLG) have been labeled by retro-grade transport of horseradish peroxidase (HRP). We studied the depth, area, and morphology of each labeled neuron quantitatively. Our measurements show that the projection neurons to both VLG and DLG vary in laminar position, size, and morphology. Labeled cells projecting to both nuclei were concentrated within the superficial gray layer, but were also scattered through the optic layer and, after DLG injections, in the intermediate gray layer as well. Labeled cells in both groups varied greatly in size, ranging from 49–344 m² cross-sectional area (mean 143 m²) for the VLG group and from 31–398 m² (mean 165 m²) for the DLG group. The labeled cells also varied in morphology after both VLG and DLG injections. The majority had a granule or vertical fusiform morphology. There were fewer with a stellate morphology and almost none with a horizontal morphology. At least three types of superior colliculus cells thus appear to project to the ventral and dorsal lateral geniculate nuclei. These cell types likely give rise to distinct functional channels to these nuclei.Abbreviations A lamina A of the dorsal lateral geniculate nucleus - A1 lamina A1 of the dorsal lateral geniculate nucleus - C lamina C of the dorsal lateral geniculate nucleus - CM central medial nucleus - CMM medial mammillary nucleus - CP cerebral peduncle - D nucleus of Darkschewitsch - FCT central tegmental tract - H habenular nuclei - HPM medial habenulo-peduncular tract - LP lateral posterior nucleus - MG medial geniculate nucleus - MIN medial intralaminar nucleus - NCP nucleus of the posterior commissure - NR reticular nucleus - OT optic tract - P pulvinar nucleus - PC posterior commissure - R red nucleus - SG suprageniculate nucleus - SN substantia nigra - VLA ventral anterolateral nucleus - VLG ventral lateral geniculate nucleus - VPL ventral posterolateral nucleus - VPM ventral postero-medial nucleus This study was supported by USPHS Research Grant EY02973 from the National Eye Institute, a New Faculty Research Grant from the State of Tennessee, and USPHS Postdoctoral Training Grant GM-00202     

Neurons with complex visual properties in the superior colliculus of the macaque monkey

Summary Single neurons were recorded from the superficial layers of the superior colliculus of immobilized monkeys (Macaca mulatta and Macaca irus). Two main functional types of neurons were found. The neurons of the first type (Type I neurons) responded well to simple stationary and moving stimuli such as spots, bars or slits of light. The latency of their response was 41 ± 6 ms. They were not directionally selective and responded to a large range of velocities.The neurons of the second type (Type II neurons) responded very poorly to simple visual stimuli and their activation required real objects or certain two-dimensional patterns. The mean latency of response of these units was 66 ± 26 ms. Habituation was always present. Type II neurons were located in the lower part of the superficial layers.The characteristics of Type II neurons suggest that in the primate superior colliculus there is a mechanism that allows the recognition of the complexity and the novelty of a stimulus and guides orienting responses to those stimuli that are worth analyzing in detail.This study was supported in part by NIH Grant 2 ROI EY00577 and in part by a grant from the Italian CNR. H.A.B. was supportet by a grant from Cassa di Risparmio di Parma     

Origin of high acetylcholinesterase activity in the mouse superior colliculus

Summary The acetylcholinesterase activity in the colliculus mainly occurs in two layers and is arranged as a lattice in the intermediate grey layer and as a continuous sheet in the superficial grey layer. Under-cutting lesions abolish the lattice in the intermediate grey layer but leave the superficial sheet of activity intact. By contrast the injection of kainic acid into the colliculus leaves the intermediate layer lattice intact while causing a local reduction in the superficial layer. Injections of the retrograde tracer Fluoro-Gold into the colliculus labels cells in the pedunculopontine and laterodorsal tegmental nuclei that contain acetylcholinesterase. Cells in the parabigeminal nucleus are also labelled but these cells contain low levels of cholinesterase. Thus, it is concluded that the lattice in the intermediate layers is mainly dependent on afferents from the laterodorsal tegmental and pedunculopontine nuclei while the sheet in the superficial layers is mainly dependent on intrinsic cells.     

Cross-correlated and oscillatory visual responses of superficial-layer and tecto-reticular neurones in cat superior colliculus

The present study examined, in the superior colliculus (SC) of anaesthetised cats, the functional connectivity between superficial-layer neurones (SLNs) and tectoreticular neurones (TRNs: collicular output cells). TRNs were antidromically identified by electrical stimulation of the predorsal bundle. The auto- and cross-correlation histograms of visual responses of both types of neurones were recorded and analysed. A delayed, sharp peak in cross-correlograms allowed us to verify whether SLN and TRN cells were coupled; in addition, oscillatory activities were compared to verify if rhythmic responses of SLN sites were transmitted to TRN sites. We found that oscillatory activity was rarely observed in spontaneous activity of superficial (1/74) and TRN sites (1/48). Moving light bars induced oscillation in 31% (23/74) of the superficial-layer and in 23% (11/48) of the TRN sites. The strength of the rhythmic responses was determined by specific ranges of stimulus velocity in 83% (19/23) and 64% (7/11) of oscillating SLN and TRN sites, respectively. Frequencies of oscillations ranged between 5 and 125 Hz and were confined, for 53% of the cells, to the 5-20 Hz band. Thus, the band-width of frequencies of the stimulus-related oscillations in the superior colliculus was broader than the gamma range. Analysis of cross-correlation histograms revealed a significant predominant peak with a mean delay of 2.7+/-0.9 ms in 46% (17/37) of SLN-TRN pairs. Most correlated SLN-TRN pairs (88%: 15/17) had superimposed receptive fields, suggesting they were functionally interconnected. However, individual oscillatory frequencies of correlated and oscillatory SLN and TRN cells were never the same (0/8). Together, these results suggest that the neurones in collicular superficial layer contact TRNs and, consequently, support the idea that the superficial layers contribute to collicular outputs producing eye- and head-orienting movements.     

Dissociation of stimulation-bound feeding and apomorphine-induced gnawing by lesions of superior colliculus

The intense stereotyped gnawing induced by high doses of apomorphine is almost abolished by large bilateral lesions of the superior colliculus. It has been argued that the feeding produced by electrical stimulation of the lateral hypothalamic area is closely related to dopamine-mediated oral stereotypies; if so, it might be expected that lesions of the superior colliculus would also disrupt stimulation-bound feeding. Feeding was obtained from 14 hypothalamic electrodes in 8 hooded Lister rats. Subsequent electrolytic lesions of the superior colliculus had no overall effect on this behaviour from 13 of the 14 electrodes, even though the lesions reduced the gnawing induced by 8–20 mg/kg apomorphine to less than 10% of its preoperative intensity. It is concluded that stimulation-bound feeding and apomorphine-induced gnawing are not dependent on identical neural circuitry, and therefore stimulation-bound feeding is probably not mediated by the nigrotectal pathway.     

Effects on visual search of lesions of the superior colliculus in infant or adult rats

Summary The superior colliculus was removed from rats at either one or five days of age or in maturity. Four months later they were tested on two versions of a visual search task. Experiment 1 required animals to retrieve food pellets concealed in a depression in the top of identical narrow pillars arranged in an arena. Rats with lesions of the superior colliculus, regardless of the age at operation, showed a large number of return errors compared with sham-operated controls. Return errors were defined as occasions on which the animal returned to pillars that had previously been visited on that trial, before every pillar had been visited at least once. Experiment 2 compared the ability of infantand adult-operated animals to detect and locate a single, baited white pillar in an array of black ones. There were no group differences in response latencies to targets presented in the rostral visual field (within 40° of the midline). However, animals operated on in adulthood or at 5 days of age were slower than both sham-operated animals and animals operated on at one day of age in their responses to more peripheral targets. The latter two groups were indistinguishable.