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R B Illing

Publications and source records attributed to R B Illing.

At least 19 recordsLinked to original sources

Re-emergence of GAP-43 in cochlear nucleus and superior olive following cochlear ablation in the rat.

The effect of cochlear lesion on the expression of the growth associated protein GAP-43 in superior olive and cochlear nucleus was studied in the rat. In normal development of these auditory brainstem nuclei, GAP-43 immunoreactivity is high perinatally but low 10 days postnatally or thereafter. Removal of one spiral ganglion in grown-up animals caused a substantial re-emergence of GAP-43 immunoreactivity in varicose fibers of the ipsilateral ventral cochlear nucleus and cell bodies of the lateral superior olive. These findings suggest that a reactive synaptogenesis takes place in the cochlear nucleus as a consequence of deafening through spiral ganglion loss.

Animals

Enkephalin-positive and acetylcholinesterase-positive patch systems in the superior colliculus have matching distributions but distinct developmental histories.

Histochemical stains for acetylcholinesterase activity and enkephalin-like immunoreactivity both demonstrate a high degree of patterning in the superior colliculus, particularly in the intermediate and deep layers. Both markers occur predominantly in the neuropil of these layers, and both are principally distributed in distinct macroscopic compartments. We report here that patches of heightened acetylcholinesterase activity correspond to patches of high enkephalin-like immunoreactivity. The two markers thus delineate largely the same domain in the intermediate and deep layers. The most prominent zones of staining for enkephalin-like peptide and for acetylcholinesterase also coincided in the dorsolateral periaqueductal gray matter. These findings suggest a close interlocking of one or more acetylcholinesterase-containing systems with one or more pathways related to endogenous opioids in the superior colliculus. As the acetylcholinesterase expression in the patches is known to match in detail choline acetyltransferase expression, our results also suggest the possibility of local cholinergic-opiatergic interactions. In some sections, blood vessels associated with enkephalin-rich and acetylcholinesterase-rich patches extended beyond the colliculus into the periaqueductal gray matter, where they again became surrounded by dense fibrous labeling. This pattern suggests that neurohumoral signal exchange might occur through blood vessels even in a sensory-motor structure such as the colliculus. In a postnatal developmental series of kitten brains we found that enkephalin-like immunoreactivity was already distinctly compartmental in the intermediate layers at birth and continued to show this distribution throughout postnatal development. By contrast, acetylcholinesterase staining was nearly homogeneous at birth and became compartmental gradually during the first postnatal weeks. Thus, despite the eventual near coincidence of the enkephalin-rich and acetylcholinesterase-rich compartments of the superior colliculus, they mark systems that follow distinct programs of neurochemical development.

Acetylcholinesterase

Pattern formation in the developing superior colliculus: ontogeny of the periodic architecture in the intermediate layers.

The superior colliculus of mammals contains a striking neurochemical architecture in which histochemically identifiable compartments are distributed in an iterative arrangement in the intermediate layers. We used stains for acetylcholinesterase activity as a compartment marker to trace ontogenesis of this architecture during pre- and postnatal development in the domestic cat. We found that compartmentation in the intermediate collicular layers is virtually absent at birth, and only gradually emerges during the first weeks of postnatal life. Over the same postnatal period, acetylcholinesterase activity shifts from a predominantly perikaryal expression pattern immediately postnatally to a nearly exclusive localization in the neuropil at maturity. Remarkably, a striking compartmentation of the superior colliculus was readily apparent with acetylcholinesterase histochemistry prenatally. The first appearance of a periodic architecture in the superior colliculus was observed at embryonic day 34, a time at which the collicular plate had not yet become laminated. The compartments characterized by high levels of acetylcholinesterase activity then gained in prominence until late in the prenatal period, when they receded and disappeared. The loss of the acetylcholinesterase-positive compartments in the perinatal period did not reflect a loss of compartmentation altogether. Neonatally, there was a distinct compartmental architecture visible with enkephalin immunohistochemistry. The virtual absence of acetylcholinesterase-positive compartments in the superior colliculus at birth therefore reflects developmental regulation of enzyme expression in the compartments, not regulation of the compartments as structural entities. We conclude that the periodic architecture, which characterizes the intermediate collicular layers in the adult cat, arises early in ontogenesis. These observations raise the possibility that the histochemical compartments are ontogenetic units that undergo remodeling as the superior colliculus matures.

Acetylcholinesterase

Distribution of cytochrome oxidase and parvalbumin in the primary visual cortex of the adult and neonate monkey, Callithrix jacchus.

The anatomical distributions of the mitochondrial enzyme cytochrome oxidase (CO) and of the calcium binding protein parvalbumin (PV) were studied in the striate cortex of adult and neonate New World monkeys (Callithrix jacchus). In the adult marmoset, both proteins were found in laminar arrangements similar to those described for the macaque monkey, with prominent bands of PV-like immunoreactive (PV-LI) puncta in layers IV and IIIb, and fairly evenly distributed PV-LI nonpyramidal neurons. Furthermore, the pattern of CO activity in area 17 of the neonate marmoset was almost identical to the CO pattern described in neonate macaque and squirrel monkeys. It came, therefore, as a surprise to find that the adult pattern of PV-like immunoreactivity (PV-LI) in the marmoset striate cortex arises from a neonatal pattern strikingly different from that seen in any developmental stage of the macaque, or in any other mammal studied so far. In the deep layers IV through VI of the neonate marmoset, a large number of PV-LI neurons was stained in bandlike patterns, their number in layers IV and V exceeding the number of PV-LI neurons present in these layers of the adult marmoset area 17. Staining of layers IV and VI was restricted to area 17 and involved nonpyramidal cells and their processes. The stained band of layer V, in contrast, continued throughout most of the neocortex. In area 17, an estimated 10 to 20% of the stained cells in layer V exhibited pyramidal shapes. The findings show that the expression of PV by visual cortical cells occurs before birth and suggest that the comparatively early onset of PV expression is not dependent on the onset of textured vision. The exuberant number of stained cells in some layers, and particularly the staining of pyramidal cells, in the neonate marmoset, suggest that a considerable number of cells possesses the stainability for PV-LI only transiently, i.e., in the marmoset, these cells have a specific demand for parvalbumin during this phase of their development.

Animals

Distribution of cytochrome oxidase in layers IV and V of the striate cortex in neonate monkeys.

The uniformly dense staining for cytochrome oxidase (CO) in layer IV of area 17 in adult monkeys has been described as developing from a bilaminar pattern in neonates being composed of a broad CO band in layer IV alpha and a narrow CO band attributed to the innermost zone of layer IV beta. Here we present evidence, in the neonate marmoset monkey, for the narrow CO band to be localized in the outermost rim of layer V, designated as sublayer Va.

Aging

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Animals

Association of efferent neurons to the compartmental architecture of the superior colliculus.

The superior colliculus is a layered structure in the mammalian midbrain serving multimodal sensorimotor integration. Its intermediate layers are characterized by a compartmental architecture. These compartments are apparent through the clustering of terminals of major collicular afferents, which in many instances match the heterogeneous distribution of tissue components such as acetylcholinesterase, choline acetyltransferase, substance P, and parvalbumin. The present study was undertaken to determine whether efferent cells observe this compartmental architecture. It was found that subpopulations of both descending and ascending collicular efferents originate from perikarya situated in characteristic positions relative to the collicular compartments defined by elevated acetylcholinesterase activity and that their dendrites appear to be specifically coordinated with the heterogeneous environment. With the specific interlocking of afferent and efferent neurons through spatially distinguished neural networks, the compartmental architecture apparently constitutes an essential element for the determination of information flow in the superior colliculus.

Acetylcholinesterase

Similarities and differences between cholinergic systems in the superior colliculus of guinea pig and rat.

We studied the distribution of acetylcholinesterase activity and choline acetyltransferase immunoreactivity in the superior colliculus of the guinea pig and the albino rat, using enzyme histochemical and immunohistochemical methods. Choline acetyltransferase-like immunoreactivity was localized in the neuropil throughout the colliculi, but the density of the immunoreactive neuropil varied among layers as well as between species. In the intermediate collicular layers the pattern of choline acetyltransferase immunoreactivity was closely matched by the distribution of acetylcholinesterase activity in guinea pig and rat, confirming our previous findings in the cat. Furthermore, in the guinea pig, but not in the rat, choline acetyltransferase-like immunoreactivity was localized in a prominent population of perikarya of the superficial gray layer.

Acetylcholinesterase

Delineation of the striate cortex, and the striate-peristriate projections in the guinea pig.

The size and position of the guinea pig area 17 were determined by transneuronal labeling after intraocular injections of 3H-proline or WGA-HRP. Area 17 occupies a large region of the occipital cortex located between two shallow fissures, the fissura sagittalis lateralis and the lateral groove. Area 17 extends for about 6 mm rostral from the occipital pole of the hemisphere, and encroaches occipitally for more than 1 mm upon the ventromedial surface of the hemisphere; the lateral width is up to 4.5 mm. Single injections of WGA-HRP into area 17 produced eight patches of transported tracer which formed the same general pattern in the peristriate cortex, regardless of the position of the injection within the visual field representation of area 17. Two of these patches were found in anteromedial peristriate cortex; three patches were distributed anterolateral and lateral of area 17; and three patches were located in posterolateral peristriate cortex. For several reasons, each of these patches was interpreted as representing a single striate projection onto a separate peristriate area. Comparison of these results with published findings indicates that the parcellation of the peristriate cortex into a variety of different areas, the pattern formed by these areas around area 17, and their reciprocal connections with area 17 follow a common plan in all hitherto studied terrestrial Old World and New World rodents. Lucifer Yellow injections into striate cells projecting to one of the recipient areas (AM) indicated that the pyramidal cells of this set of striate neurons are characterized by a short apical dendrite, and that the basal dendrites of the layer V pyramidal cells branch more profusely than those of the layer III pyramids.

Animals

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.

Acetylcholinesterase

A subtype of cerebellar Golgi cells may be cholinergic.

In cerebellar sections of the feline brain processed for choline acetyltransferase-like immunoreactivity, a population of distinctly stained cells was discovered in the granular layer of the cortex in both vermis and hemispheres. Their position and morphology qualify them as Golgi cells, but their density indicated that they comprise less than 5% of all cerebellar Golgi cells. Varicose immunoreactive fiber nets in all cortical layers also contribute to seemingly widespread cholinergic systems in the cerebellar cortex.

Animals

Choline acetyltransferase-like immunoreactivity in the superior colliculus of the cat and its relation to the pattern of acetylcholinesterase staining.

Choline acetyltransferase, the biosynthetic enzyme for acetylcholine, is thought to be a marker for cholinergic neurons. This report presents an analysis of the pattern of choline acetyltransferase-like immunoreactivity in the superior colliculus of the cat. A dense network of highly varicose immunoreactive fibers pervaded the superficial gray and optical layer. The density of the fiber network in the superficial layers was heterogeneous, forming a mosaic pattern with a period of about 400 microns. The antigen was also located in numerous small perikarya embedded in this network. This neuronal population reached a density of 2,000 cells/mm3 of the superficial gray layer and suggested the presence of a substantial cholinergic system originating in the superior colliculus. A detailed comparison was made between the pattern of choline acetyltransferase-like immunoreactivity and the distribution of acetylcholinesterase activity. By comparisons of adjacent sections, both staining patterns were found to be similar in all collicular layers. In particular, the compartmental distribution of immunoreactivity in the intermediate collicular layers seemed to mimic the pattern of acetylcholinesterase staining. A double-staining technique demonstrated a near-perfect correlation between the two patterns. In conclusion, there was no indication of heightened acetylcholinesterase activity without an associated elevation in choline acetyltransferase-like immunoreactivity throughout the superior colliculus. In this part of the brain, the presence of the putative cholinergic terminals could fully account for the distribution of acetylcholinesterase activity.

Acetylcholinesterase

Release of met-enkephalin and its modulation through acetylcholine receptors in the rabbit superior colliculus.

This report presents evidence for the depolarization-dependent release of met-enkephalin from the superior colliculus of the rabbit. Collicular tissue was placed in superfusion chambers and met-enkephalin accumulation in the superfusate was measured by radioimmunoassay. Exposure to high potassium concentrations (30 mM and 56 mM) increased met-enkephalin release. This is the fourth transmitter shown to be released from collicular tissue. Furthermore, we have obtained the first evidence that suggests that met-enkephalin release is susceptible to muscarinic modulation. While the depolarization-dependent release of met-enkephalin was depressed in the presence of atropine (1 microM), hexamethonium (100 microM) did not block the increase of met-enkephalin release induced by high potassium.

Animals

The mosaic of the uncrossed retinal projection in the superior colliculus of the cat.

The uncrossed retinocollicular projection in the cat was labeled by axonal transport of horseradish peroxidase from the eye and visualized in tangential sections through the superior colliculus. The terminals of this pathway are distributed in clusters and form a mosaic pattern rather than stripes in the superficial collicular layers. It is suggested that the periodicity of this pattern relates to the smallest receptive field diameters across the visual field.

Animals

Macro square wave jerks in a rhesus monkey: physiological and anatomical findings in a case of selective impairment of attentive fixation.

An otherwise normal female rhesus monkey executed large saccadic eye movements (macro square wave jerks) when required to attentively fixate a small visual target (fixation point). The jerks were observed exclusively in this specific testing situation. They occurred periodically at a frequency of 2.04 + - 0.18 Hz to the right side with an amplitude of 23.5 deg. Direction of the jerks was about 3-4 degrees downward from horizontal. These parameters remained constant throughout the several months of daily recording. No jerks were executed during periods when the behaviourally important target was absent or substituted by another, behaviourally non-relevant visual stimulus. The monkey could perform normal visually guided saccades as well as smooth pursuit eye movements, but with the jerks always superimposed, when the monkey paid attention to the visual target. Histologic inspection of the brain revealed the presence of an incapsulated nematode in the cortex of lobulus simplex of the right cerebellar hemisphere, i.e., in a region involved in oculomotor control.

Animals

Spatial relation of the acetylcholinesterase-rich domain to the visual topography in the feline superior colliculus.

The superior colliculus (SC) of the cat shows a prominent compartmentalized organization at the level of its intermediate layers. The mosaic of these compartments is apparent in the pattern of acetylcholinesterase (AChE) staining. Patches of high AChE-activity are sharply set off from surrounding areas in the caudal SC while they are less distinct anteriorly. The rostral part lacks such obvious compartments. Thus, a structural reorganization apparently cuts across the topographical representations spread out in the SC. In order to test if this compartmental gradient relates to the topographic maps of the colliculus, retinotopic landmarks were visualized in the superficial layers by labeling the retinotectal pathway. In the SC ipsilateral to the eye injected with horseradish peroxidase (HRP) a paucity of labeling indicated the zone representing the ipsilateral visual half-field. Serial reconstructions of collicular sections, cut longitudinally or tangentially, revealed that the non-compartmentalized part of the intermediate layers corresponds to the representation of the ipsilateral visual half-field in the layers above, while an intricate mosaic array of compartments prevail in tectal zones related to the representation of the contralateral visual half-field.

Acetylcholinesterase

Evidence for a neurotransmitter function of acetylcholine in rabbit superior colliculus.

Acetylcholinesterase staining and studies on the uptake of [3H]choline into the subsequent efflux of tritium from collicular slices were carried out in order to provide evidence for a neurotransmitter function of acetylcholine in rabbit superior colliculus. Acetylcholinesterase staining was dense and homogeneous in superficial layers whereas the staining was arranged in patches with slightly higher density caudally than rostrally in the intermediate layers. The accumulation of tritium in slices incubated with [3H]choline depended on time, temperature and concentration, and was inhibited by hemicholinium-3. Accumulation was slightly higher in caudal than in rostral slices. Electrical stimulation enhanced tritium outflow from slices preincubated with [3H]choline. Tetrodotoxin and a low calcium medium inhibited the evoked overflow whereas hemicholinium-3 caused an enhancement. Oxotremorine decreased the evoked overflow; atropine prevented this effect. The opioids [D-Ala2, MePhe4, Glycol5]enkephalin, [D-Ala2, D-Leu5]enkephalin and ethylketocyclazocine caused an inhibition. The effects of the latter two agonists were antagonized by naloxone. The GABAB-receptor-agonist (-)-baclofen decreased the evoked overflow at lower concentrations than GABA, whereas the GABAA-receptor-agonist muscimol was ineffective. Serotonin produced an inhibition which was prevented by metitepin, alpha- and beta-adrenoceptor as well as dopamine-receptor ligands caused no change. It is concluded that in the rabbit superior colliculus the pattern of acetylcholinesterase staining is comparable, but not identical to the distribution in other species. The accumulation of [3H]choline, as well as the tetrodotoxin-sensitive and calcium-dependent overflow of tritium upon electrical stimulation (reflecting presumably release of [3H]acetylcholine) indicate that acetylcholine has a neurotransmitter function in this tissue. The release of [3H]acetylcholine was modulated by various transmitter substances and related compounds. The pattern of modulation of release differed from the pattern in other cholinergically innervated tissues.

Acetylcholine

Complementary and non-matching afferent compartments in the cat's superior colliculus: innervation of the acetylcholinesterase-poor domain of the intermediate gray layer.

Three tectal afferent-fiber systems were experimentally labeled in the cat to learn how their distributions within the superior colliculus were related to the prominent compartments of high acetylcholinesterase activity found in the intermediate gray layer. Presumptive somatic sensory afferents were labeled by injections of horseradish peroxidase-wheatgerm agglutinin conjugate placed at the bulbospinal junction and in the ventral anterior ectosylvian cortex corresponding to somatic sensory area SIV. Vision-related afferents were labeled by injections of the same tracer substance into the lateral suprasylvian visual area. In each animal, a single type of injection was made and a detailed study was carried out to compare the patterns of anterograde labeling and acetylcholinesterase staining in serially adjoining sections through the superior colliculus. Fibers labeled by the three types of injection were distributed in clusters that resembled the acetylcholinesterase-positive patches in the intermediate gray layer. In no case, however, were the afferent-fiber clusters in register with the histochemically defined patches. Instead, the innervations derived from the bulbospinal junction, anterior estosylvian sulcus and lateral suprasylvian visual area all formed patchworks within the acetylcholinesterase-poor domain of the intermediate gray layer. In some instances, the afferent-fiber clusters and enzyme-positive patches appeared to have complementary distributions. In other instances, the afferent-fiber clusters seemed to be arranged in the acetylcholinesterase-poor parts of the intermediate layer in a fashion independent of, but not significantly overlapping, the acetylcholinesterase-positive patches. Not all of the space between the acetylcholinesterase-positive patches was taken up by any one of the afferent-fiber systems labeled. The complementary and non-matching distribution of these afferent systems in relation to the acetylcholinesterase-rich patches of the intermediate gray layer stands in contrast to the spatial registration of two other tectal afferent systems with the zones of high acetylcholinesterase activity. Both nigrotectal and frontotectal afferents converge on the acetylcholinesterase-positive patches. We conclude that afferent systems projecting to the intermediate gray layer can be divided into at least two groups: those innervating the acetylcholinesterase-rich compartments and those avoiding them.(ABSTRACT TRUNCATED AT 400 WORDS)

Acetylcholinesterase