Parvalbumin in rat superior colliculus

Parvalbumin-like immunoreactivity (PA-LI) has been studied in sections of the superior colliculus (SC) of the rat and its distribution compared to the patterns of acetylcholinesterase (AChE) and cytochrome oxidase (CO) staining. In the intermediate layers it was found that PA-LI is spatially associated with AChE only in the medial part of the SC, but assumes a complementary distribution further laterally. There was a positive correlation between PA-LI and CO. We conclude that the patterns of PA-LI and CO are not systematically related to collicular input known to be associated with the AChE-rich zones, but may reflect adherence to channel separation beyond the terminal fields of clustered afferents.     

Nociceptive neurones in rat superior colliculus

Accumulating evidence suggests that the rodent superior colliculus (SC) plays as important a role in avoidance and defensive behaviours as it does in orientation and approach. These two complementary behaviours are associated with two anatomically segregated tectofugal output pathways, such that orientation and approach are mediated by the crossed descending projection, whereas avoidance and defence are subserved via the uncrossed projection. Because nociceptive neurones in the SC have been presumed to participate in withdrawal or defensive behaviours, it has been proposed that they have direct access only to the uncrossed efferent pathway. However, in certain behavioural situations, the most adaptive response to injury, or to a painful object in prolonged contact with the skin, is to orient towards the source of discomfort so that the skin can be licked and/or the offending object removed. Presumably then, nociceptive as well as low-threshold neurones would have access to the crossed descending pathway in order to initiate such behaviours. Determining whether or not this is the case was the objective of the present study. Both nociceptive-specific (82%) and wide-dynamic-range (18%) SC neurones were identified using long-duration (up to 6 s), frankly noxious mechanical and thermal stimuli in urethane-anaesthetised Long-Evans hooded rats. The majority (85.7%) of the nociceptive neurones encountered were located within the intermediate layers, which corresponds with the location of the cells-of-origin of the crossed descending projection. Nearly half (44.9%) were activated antidromically from electrical stimulation of the crossed descending pathway at a site in the brainstem below its decussation. The mean conduction velocity of these nociceptive output neurones was 9.02 m/s, which corresponds well to previous estimates of conduction velocity in the crossed tecto-reticulo-spinal tract. These data demonstrate that a significant proportion of nociceptive neurones in the rat SC have axons that project to the contralateral brainstem via the crossed descending projection. Nociceptive neurones could, therefore, effect orientation responses to noxious stimuli via similar output pathways that low-threshold neurones utilize to initiate orientation to innocuous stimuli.     

The direct visuo-motor pathway in mammalian superior colliculus; novel perspective on the interlaminar connection

The mammalian superior colliculus (SC) is a center controlling the orienting behaviors such as saccadic eye movements. The superficial layers receive visual inputs and the deeper layers send descending motor command to the brainstem and spinal cord. Existence of the interlaminar connection from the superficial to the deeper layers has been an issue of debate during the last two decades. Recent studies have proved the existence of the interlaminar connection by introducing the in vitro slice preparations. When the collicular circuit is disinhibited from gamma-amino butyric acid A (GABA(A)) receptor-mediated inhibition, the signal transmission through the interlaminar connection is enormously facilitated and neurons in the deeper layers exhibit bursting response to stimulation of the superficial layer with non-linear amplification mechanism that depends on the activation of NMDA-type glutamate receptors. In addition, the cholinergic input to the intermediate layer lowers the threshold for the bursting response and facilitates the transmission through the interlaminar connection via activation of nicotinic receptors. The signal transmission through the interlaminar connection may lead to execution of extremely short latency saccades called express saccades.     

Projections from auditory structures to the superior colliculus in the rat

Arginine-vasopressin (AVP) and related peptides were administered by microinjection into the nucleus tractus solitarius of the rat. AVP produced a rise both in mean arterial pressure and in heart rate. This effect was abolished by pretreatment with a specific antagonist of V1 receptors and was not seen either after injections of oxytocin or of the V2 agonist deamino-D-arginine-vasopressin. This study provides evidence for a specific action of vasopressin on the cardiovascular system in the nucleus of the tractus solitarius, which is mediated neither by V2 nor oxytocin receptors.     

Ionic mechanisms of GABA-induced long-term potentiation in the rat superior colliculus

GABA-induced excitation and long-term potentiation (LTPG) have been demonstrated recently in the superficial layers of the superior colliculus (SC). In other regions of the nervous system, GABA elicits excitatory responses via ionotropic GABA receptors under certain conditions. This excitation is proposed to be due to either a high neuronal chloride concentration favouring a depolarising chloride efflux, or to a bicarbonate efflux coupled to a chloride influx. The aim of this study was to characterise the mechanisms underlying excitation and prolonged increase in synaptic transmission induced by GABA in the SC. Extracellular field potentials were recorded from 1-month-old rat SC slices, and LTPG of these responses was evoked by application of 3 mM GABA. GABA-induced excitation and LTPG were significantly reduced by lowering the extracellular calcium concentration, but not by a decreased potassium concentration. Replacing the extracellular bicarbonate-buffered perfusion medium with a HEPES-buffered solution had no effect on LTPG but blocking the bicarbonate-generating enzyme carbonic anhydrase both intra- and extracellularly with ethoxyzolamide (50 microM) prevented LTPG. The chloride transport inhibitor bumetanide (50 microM) reduced but did not block LTPG. We therefore suggest that the contribution of the chloride equilibrium to LTPG is only of minor importance. The intracellular bicarbonate pool and related efflux provides the basis for the excitatory action of GABA, leading to a subsequent depolarisation and calcium influx through voltage-dependent calcium channels, thus causing long-lasting changes in synaptic transmission.     

Postnatal alterations of GABA receptor profiles in the rat superior colliculus

Midbrain sections taken from Sprague-Dawley rats of varying ages within the first four postnatal weeks were used to determine, immunocytochemically, putative changes of GABA(A) receptor beta2/3 subunits, GABA(B) receptor (R1a and R1b splice variants), and GABA(C) receptor rho1 subunit expression and distribution in the superficial, visual layers of the superior colliculus. Immunoreactivity for the GABA(A) receptor beta2/3 subunits was found in the superficial grey layer from birth. The labelling changed with age, with an overall continuous reduction in the number of cells labelled and a significant increase in the labelling intensity distribution (neuropil vs soma). Further analysis revealed an initial increase in the labelling intensity between postnatal days 0 and 7 in parallel with an overall reduction of labelled neurones. This was followed by a significant decrease in labelling intensity distribution between postnatal days 7 and 16, and a subsequent increase in intensity between postnatal days 16 and 28. The labelling profiles for GABA(B) receptors (R1a and R1b splice variants) and GABA(C) receptors (rho1 subunit) showed similar patterns. Both receptors could be found in the superficial layers of the superior colliculus from birth, and the intensity and distribution of labelling remained constant during the first postnatal month. However, the cell body count showed a significant decrease between postnatal days 7 and 16. These changes may be related to the time-point of eye opening, which occurred approximately two weeks after birth. For all three receptor types, the cell body count remained constant after postnatal day 16. By four weeks of age, there was no significant difference between the cell numbers obtained for the different receptors. Both GABA itself and neurofilament labelling were also obtained in the superficial superior colliculus at birth. Neurofilament, although found at birth, showed very little ordered arrangement until 16days after birth. When slices were double labelled for GABA(C) receptors and neurofilament, some overlap was observed. Double labelling for the presynaptic protein synaptophysin and GABA(C) receptors showed proximity in some places, indicative of a partly synaptic location of GABA(C) receptors. When GABA(C) and GABA(A) receptors were labelled simultaneously, some but not all neurones showed immunoreactivity for both receptor types.In conclusion, all three GABA receptor types were found to be present in the superior colliculus from birth, and all show some form of postnatal modification, with GABA(A) receptors demonstrating the most dramatic changes. However, GABA(B) and GABA(C) receptors are modified significantly around the onset of input-specific activity. Together, this points towards a contribution of the GABAergic system to processes of postnatal maturation in the superficial superior colliculus.     

Effects of superior colliculus ablation on the air-righting reflex in the rat

To examine how the superior colliculus, the motor center of orientation and avoidance, could interact with postural reflexes, we investigated effects of unilateral and bilateral ablations on air-righting reflex movements in otherwise intact rats. Superior colliculus ablations variously modified righting movements: After falling from the supine position, the rats sometimes showed dorsiflexion instead of normal ventriflexion; the motor sequence of rotation from the fore- to the hindquarter was often modified to simultaneous rotation; lateral turn from supine to prone position was occasionally insufficient; body direction that was normally kept constant during falling was often changed; final posture sometimes deviated from the horizontal position. The first three abnormalities occurred almost twice in frequency as lesions increased from unilateral to bilateral ablation, and in unilaterally ablated rats, did so in righting contraversive to the lesions. Multiple influences of tectoreticular input to the air-righting reflex center are discussed.     

Cholinergic responses in crossed tecto-reticular neurons of rat superior colliculus

Neurons in the intermediate gray layer (SGI) of mammalian superior colliculus (SC) receive cholinergic innervation from the brain stem parabrachial region, which seems to modulate the signal processing in the SC. To clarify its role particularly in orienting behaviors, we studied cholinergic effects on the major output neuron group of the SGI, crossed tecto-reticular neurons (cTRNs), identified by retrograde labeling from the contralateral brain stem gaze center in SC slices obtained from rats (PND 17-22) by whole cell patch-clamp techniques. Bath application of carbachol induced either 1) nicotinic inward (nIN) + muscarinic inward (mIN) (11/24) or 2) nIN + mIN + muscarinic outward (mOUT) (13/24) current responses. Transient pressure application of 1 mM acetylcholine elicited nIN in all neurons tested (n = 58). In a majority of these neurons (52/58), the nIN was completely suppressed by dihydro-beta-erythroidine, a specific antagonist for alpha4beta2 nicotinic receptor subtype. The remaining 6/58 neurons exhibited not only the slower alpha4beta2 receptor-mediated component but also a faster component that was inhibited by a specific antagonist for alpha7 nicotinic receptor, alpha-bungarotoxin. cTRNs expressing alpha7 nicotinic receptors tended to be smaller in size than those lacking alpha7 receptors. Bath application of muscarine induced two response patterns: mIN only (17/38) and mIN+ mOUT (21/38). The mIN and mOUT were mediated by M3 (plus M1) and M2 muscarinic receptors, respectively. These results suggest that a major response to cholinergic inputs to cTRNs is excitatory. This would indicate the facilitatory role of the brain stem cholinergic system in the execution of orienting behaviors including saccadic eye movements.     

Uncrossed retinal fibers terminating in the superior colliculus of the albino rat

The site of termination of uncrossed retinal fibers was examined in the superior colliculus of the albino rat. Sixty-eight male and female rats of Gifu, Donryu, Wistar and Sprague-Dawley strains from 9 days to 24 months of age were examined by means of a silver impregnation method for degenerating nerve fibers and the horseradish peroxidase method. In this study, terminals of uncrossed retinal fibers were observed in a small region from the posteromedial to the posterior part of the superficial gray stratum of the ipsilateral superior colliculus.     

The projection from superior colliculus to cuneiform area in the rat

Although the ipsilateral descending pathway is a major output projection of the superior colliculus, little is known of its functions. We therefore carried out two studies to investigate in rats the part of the ipsilateral projection that terminates in an area ventral to the inferior colliculus, referred to as the cuneiform nucleus. The first study, described here, used orthograde and retrograde tract-tracing techniques to locate the cells of origin and precise region of termination of the tectocuneiform pathway. The main findings were as follows. Injections of WGA-HRP into the superior colliculus gave terminal label in the cuneiform nucleus and also in surrounding structures which included central grey, the midbrain tegmentum bordering the parabigeminal nucleus, and the external nucleus of the inferior colliculus. As well as the strong ipsilateral projection, there was a much weaker contralateral one which crossed the midline in the tectal commissure. Label in the cuneiform nucleus was heaviest after injections into the medial deep layers. However, no clear evidence was found for topography within the tectocuneiform projection: cuneiform label varied in intensity rather than pattern of distribution with variation in the collicular location of the injection site. Injections of retrograde tracers into the cuneiform are a labelled large numbers of collicular cells, which were distributed mainly in the deep and intermediate grey layers. In agreement with the data from orthograde tracing, the heaviest concentration of labelled cells was found in the medial deep layers. This concentration extended into the adjacent dorsolateral part of central grey. A similar distribution of labelled cells was seen after injections into the structures next to the cuneiform nucleus that also receive a tectal projection. Comparison of this distribution with that obtained from injections into other parts of the ipsilateral projection, including dorsolateral basilar pons, suggested that the projection to the cuneiform area may arise from a distinct set of collicular output cells. The projection from the superior colliculus to the cuneiform nucleus and immediately adjacent areas may therefore be also functionally distinct, mediating a particular kind of tectally-elicited response. The lack of clear topography in the projection suggests that this response may not have precise spatial direction.(ABSTRACT TRUNCATED AT 400 WORDS)     

The projection from superior colliculus to cuneiform area in the rat

Summary To investigate the role of the projection from superior colliculus to the cuneiform nucleus in mediating collicular responses, the cuneiform area (including the cuneiform nucleus and immediately adjacent structures such as caudal central grey) was stimulated in rats with microinjections of glutamate (50 mM, 200 nl, 10 nmole) and the animals' head and body movements observed. The most common responses obtained from sites in the cuneiform area were freezing, darting or fast running, the form or direction of which did not appear to be strongly influenced by the laterality of the injection. These responses were only a subset of those that have been obtained in previous studies from stimulation of the superior colliculus itself: stimulation of the cuneiform area did not give contralaterally directed movements resembling orienting or approach, or ipsilaterally directed movements resembling cringing or shying. It therefore appears that the tectocuneiform projection is likely to be involved only in some of the behaviours appropriate to unexpected stimuli that are mediated by the superior colliculus, namely undirected defensive responses elicited normally by certain kinds of threatening or noxious stimulation. Involvement with such responses would be consistent with an apparent lack of topography in the tectocuneiform projection, and the connections of the cuneiform nucleus with parts of the brain concerned with nociception (see previous paper). It is unclear, however, whether the somatic responses occur in parallel with, or as a result of, autonomic changes that have also been evoked by stimulation of the cuneiform area. One striking feature of stimulating the cuneiform area with glutamate was that at many sites the intensity of the response appeared to increase with successive (one to three) injections. It is possible that this plasticity of response, which can also be obtained from the superior colliculus itself, is related to processes involved in sensitisation or learning of defensive responses.     

Binocular interactions and spatial disparity sensitivity in the superior colliculus of the siamese cat

 In Siamese cats, a genetically determined massive misrouting of retinal ganglion cells toward the contralateral hemisphere, as well as an accompanying strabismus, is believed to underlie the extreme paucity of binocular cells in the primary visual cortex. However, binocular cells have been shown to be present in more important numbers at the collicular level. The present study aims at investigating binocular interactions and sensitivity to spatial disparity in the superior colliculus of the Siamese cat. The activity of single units was recorded in the superficial layers of paralyzed and anesthetized Siamese cats. Although most collicular cells were monocularly driven, a significant proportion could be driven through both eyes (34/216 or 16%). Upon isolation of a binocular cell, the receptive fields were separated, then simultaneously stimulated with two light bars. A temporal delay was introduced between the arrival of the bars in the receptive fields to generate spatial disparities (–3° to +3°, in 0.5° or 1° steps). Results showed that some binocular cells presented disparity tuning profiles similar to the tuned excitatory (12/34), tuned inhibitory (2/34), near (2/34) and far (3/34) cells found at various cortical levels in the normal cat. These interactions might allow for coarse binocular fusion as well as play a role in the initiation of vergence and the fixation of the eyes upon the appropriate plane of vision. Received: 24 March 1998 / Accepted: 24 August 1998     

Coding sound direction in noisy environment in the superior colliculus of the rat

The aim of the present study was to evaluate the effect of background noise on the directional sensitivity of neurons in the deep layers of the superior colliculus. Extra-cellular recordings were carried out in anaesthetized adult Long Evans rats. When stimulated in a noisy environment, most of the neurons remained sensitive to sound direction and only a few changed their optimal direction by more than 15°. When stimulated at their optimal direction in the presence of background noise, a majority of neurons did not modify their response rate, whereas a limited proportion of neurons showed either a significant drop or facilitation of their response rate. Moreover, the neurons’ receptive fields showed significant tuning modifications in the presence of background noise. In a noisy environment, the larger receptive fields became narrower, whereas the sharply tuned receptive fields got broader.     

Laminar specific distribution of lateral excitatory connections in the rat superior colliculus

Premovement activities in neurons in the intermediate gray layer [stratum griseum intermediale (SGI)] of the mammalian superior colliculus (SC) are essential for initiation of orienting behaviors such as saccades. Our previous study demonstrated that burst activities are induced by synchronous activation of SGI neurons communicating within a local excitatory network, which depends on NMDA-receptor-dependent synaptic transmission and release from GABAA inhibition. Furthermore, dual whole cell recordings from adjacent neurons in SGI revealed that application of 10 microM bicuculline (Bic) and reduction of extracellular Mg2+ concentration (to 0.1 mM) induce spontaneous depolarization that is synchronous between neuron pairs, suggesting the recruitment of a large number of neurons communicating through intense excitatory connections. In the present study, we investigated the properties of synchronous depolarization and the fundamental structure of the lateral excitatory network that recruits a neuronal population in SC to synchronous activation, by analyzing the synchronicity of spontaneous depolarization induced in the presence of Bic plus low Mg2+. We found that 1) spontaneous depolarization exhibits bidirectional horizontal propagation among the SGI neuron pairs; 2) induction of spontaneous depolarization is not caused by activation of intrinsic voltage-dependent conductances; 3) neurons exposed to low Mg2+ alone exhibit spontaneous depolarization, although in this case the depolarization is less synchronous; and 4) neurons exposed to Bic alone exhibit synchronous depolarization, but less frequently than those exposed to both Bic and low Mg2+. Analysis of the synchronicity of spontaneous depolarization indicates that the distribution of lateral excitatory connections is markedly different among layers of SC; the SGI neurons form extensive lateral excitatory connections, whereas they are sparse or limited within subsets of neurons in the stratum griseum superficiale (SGS). Wide-field vertical neurons in the stratum opticum have features intermediate between neurons in the SGS and SGI. Such differences in the structure of lateral excitatory connections may reflect the different way signal processing is achieved in each layer of SC.     

Organization of the neurons of origin of the descending pathways from the ferret superior colliculus

The superior colliculus (SC), through its descending projections to the brainstem and spinal cord, is involved in initiating sensory-driven orienting behaviors. Ferrets are carnivores that hunt both above and below ground using visual (and auditory) cues in the daylight but non-visual cues in darkness and in subterranean environments. The present investigation sought to determine whether the ferret SC shows organizational features similar to those found in other visually dominant animals (e.g. cats), or whether characteristics of colliculi from non-visually dominant animals (e.g. rodents) prevail. Injection of retrograde tracer into the identified targets of the colliculus (cervical spinal cord, the contralateral pontomedullary reticular formation, or the ipsilateral pontine reticular formation) labeled tectospinal, crossed tectoreticular, and ipsilateral tectoreticular neurons, respectively, within the adult ferret SC. Labeled tectospinal and crossed tectoreticular neurons were far outnumbered by neurons with ipsilateral reticular projections. Like those of their visually dominant relatives, ferret tectospinal neurons were well represented throughout the anterior-posterior extent of the SC and crossed tectoreticular neurons tended to be distributed more broadly across the intermediate gray layer than those of rodents. Thus, even though ferrets perform well as subterranean predators where non-visual cues initiate orienting behaviors, these anatomical characteristics indicate that their colliculi are organized similar to that of their visually dominant, carnivorous relatives.     

Light‐dependent retinal innervation of the rat superior colliculus

Mammalian retinal projections are divided into two anatomically and functionally distinct systems: the primary visual system, which mediates conscious visual processing, and the subcortical visual system, which mediates nonconscious responses to light. Light deprivation during a critical period in development alters the anatomy, physiology, and function of the primary visual system in many mammalian species. However, little is known about the influence of dark‐rearing on the development of the subcortical visual system. To evaluate whether the early lighting environment alters the anatomy of the subcortical visual system, we examined the retinas and retinofugal projections of rats reared in a 12:12 light/dark cycle or in constant dark from birth to 4 months of age. We found that dark‐rearing was associated with a reduction in the distribution of retinal fibers in the stratum opticum of the contralateral superior colliculus. In contrast to the plasticity of the retinocollicular projection, retinal input to sleep, circadian, and pupillary control centers in the hypothalamus, pretectum, and lateral geniculate complex was unaffected by dark‐rearing. A decrease in retinal innervation of the stratum opticum and intermediate layers of the superior colliculus may account for some of the deficits in multisensory integration that have been observed in dark‐reared animals of several species. Anat Rec 2007. © 2007 Wiley‐Liss, Inc.     

Nature of postoperative hyperactivity following lesions of the superior colliculus in the rat

Rats with deep bilateral lesions of the superior colliculus showed an increase in locomotor behaviour in the open field. In contrast, there was a decrease in head-raising, rearing, and sniffing in these animals as compared to sham-operated rats. Rats with extensive ablations of posterior neocortex were not different from the sham-operated group on any of these measures. The results are interpreted in terms of a tectoreticular inhibition of locomotion.