Ultrastructural changes in the superficial layers of the superior colliculus in Galago crassicaudatus (primates) after eye enucleation

Summary Several types of terminals were found in the three superficial collicular layers of Galago. At least two axon terminals with round vesicles (R1 and R2) could be distinguished on the basis of vesicle packing and electron density of the cytoplasmic and mitochondrial matrices. R1 axon terminals were characterized by aggregations of vesicles in an electron lucent cytoplasm and mitochondria with a relatively dark matrix, while in R2 axon terminals the vesicles were more evenly distributed in an electron dense cytoplasm and the mitochondrial matrix was pale. R2 endings occurred in clusters in the stratum griseum superficiale; they were absent in the stratum zonale. R1 endings were found in all three superficial collicular layers. Both types of R terminals made asymmetrical contacts with small dendrites, dendritic spines and F profiles. Profiles containing flattened vesicles and establishing symmetrical contacts were numerous, and many could be identified as dendrites by accepting as criteria for dendrites evenly spaced microtubules, clusters of ribosomes and the fact that these F profiles were postsynaptic to other terminals. F terminals were presynaptic to other F profiles, dendrites and somata; they were postsynaptic to R terminals and took part in serial synapses. Dendrodendritic contacts were frequent, somatodendritic contacts rare. After eye enucleation most R2 axon terminals underwent the electron dense degenerative reaction. The degeneration process was a lengthy one; many degenerating boutons were found 30 days after axotomy and some persisted up to 180 days postoperatively. There was strong indication that the superior colliculus received more crossed than uncrossed retinofugal fibers. The crossed and uncrossed retinocollicular axons terminated in two different substrata of the stratum griseum superficiale.This study was supported by N.I.H. Grant RR-00165 to Yerkes Regional Primate Research Center and N.I.H Grant EY 00638-03 to J. Tigges. — The opportunity to use the electron microscopic facilities of the Fernbank Science Center for the initial stage of this work is gratefully acknowledged.     

Physiological properties of neurons in superficial layers of superior colliculus of rabbits

Neurons in superficial layers of the superior colliculus of the rabbit are classified into three types by their electrophysiological properties. Among them, two types belong to projecting neurons which send axons to the thalamic pulvinar (N=52) and dorsal lateral geniculate nucleus (N = 54) respectively. All other neurons are pooled into the third type (N=99). Projecting neurons of both types receive monosynaptic visual inputs via optic tract fibers of similar conduction velocity, indicating that in the superior colliculus of the rabbit, there is no difference in conduction velocity between the two pathways. They also receive trisynaptic inhibitory inputs, most likely via recurrent inhibitory circuits. The third type of neurons receives disynaptic optic and trisynaptic inhibitory inputs. The function of neurons of the third type is studied.     

Auditory properties of the superior colliculus in the horseshoe bat,Rhinolophus rouxi

Summary Auditory response properties were studied in the superior colliculus (SC) of the echolocating horseshoe bat Rhinolophus rouxi, a long CF-FM bat, by the use of stationary, dichotic stimuli.The most striking finding in the horseshoe bat was an enormous overrepresentation of neurons with best frequencies in the range of the constant frequency component of the species specific echolocation call (72% of the auditory neurons). These neurons had response thresholds as low as 0 dB SPL and were narrowly tuned with Q_{10 dB} — values up to 400, just as in the nuclei of the primary auditory pathway in this species. This overrepresentation may suggest the importance of the superior colliculus in the context of echolocation behavior.While noise stimuli were not particularly effective, other auditory response properties were similar to those described in other mammals. 65% of the SC neurons in the horseshoe bat responded only to monaural stimulation of one ear, primarily the contralateral one. 32% of the neurons received monaural input from both ears. The proportion of neurons responsive to ipsilateral stimulation (41%) was rather high. Mean response latency was 8.9 ms for contralateral stimulation.A tonotopic organization is lacking, but high-frequency neurons are less frequent in rostral SC.Abbreviations CF constant frequency component of echolocation call; - >CF frequencies above range of CF-component - FM frequency modulated component of echolocation call - <FM frequencies below range of FM-component - RF resting frequency of an individual bat - Rh.r. Rhinolophus rouxi - SC superior colliculus     

Amino acid profiles in long-evans rat superior colliculus,visual cortex,and inferior colliculus

An ultransensitive triple-column ion-exchange/fluorometric method was utilized to measure the levels of over 30 amino acids and related primary amino compounds in Long-Evans rat superior colliculus (SC), visual cortex (VC) and inferior colliculus (IC). Comparison of levels of amino compounds revealed distinctly different profiles for each region. Major constituents were the neurotransmitters and related compounds glutamate, glutamine, GABA, taurine, aspartate and glycine. Glutathione levels were also relatively high in all three regions. SC exhibited a significantly higher level of GABA and -alanine compared to both VC and IC. VC had significantly higher levels of glutamate and taurine. VC exhibited the lowest level of glycine and IC the highest. A time-course experiment using SC documented that levels of eleven of thirty-four compounds, including GABA, were subject to significant postmortem alteration in vitro. SC GABA stability experiments indicated that significant in vitro increases of free GABA levels between 1 and 4 min postmortem were associated with equimolar decreases of conjugated GABA levels.     

Geometry of the superior colliculus mapping and efficient oculomotor computation

Numerous brain regions encode variables using spatial distribution of activity in neuronal maps. Their specific geometry is usually explained by sensory considerations only. We provide here, for the first time, a theory involving the motor function of the superior colliculus to explain the geometry of its maps. We use six hypotheses in accordance with neurobiology to show that linear and logarithmic mappings are the only ones compatible with the generation of saccadic motor command. This mathematical proof gives a global coherence to the neurobiological studies on which it is based. Moreover, a new solution to the problem of saccades involving both colliculi is proposed. Comparative simulations show that it is more precise than the classical one.     

Effects of the eye enucleation on the activity of monoamine oxidase and acetylcholinesterase in the superior colliculus of the rat

Summary The electron microprobe microanalyser has been used to measure the concentrations of Ca, P and S in the predentine of young rat incisors. The specimens were prepared as alcohol fixed embedded ultrathin sections, unfixed vacuum embedded dry cut ultrathin sections and as thin cryostat sections. The results show the influence of preparation on the measured compositions and indicate that Ca is tightly bound to the matrix, whereas P can be easily washed out. Measurements along the dentine-predentine border demonstrated zones of Ca enrichment, the average size of which suggests that the zones could be the prestages of calcospherites. A mineralisation mechanism is discussed in which the high Ca concentration activates pyrophosphatase or ATPase before the onset of nucleation.The authors express their thanks to the Deutsche Forschungsgemeinschaft for financial support     

The synaptic distribution of the retinal input in the superficial layers of the guinea-pig superior colliculus

An evoked potential consisting of four postsynaptic components was recorded in the guinea-pig superior colliculus following electrical stimulation of the contralateral optic nerve. This potential was generated in response to the activation of four populations of optic nerve fibres with different conduction velocities. Current source-density analysis revealed that the two slower conducting fibre populations synapse in the upper third of the stratum griseum superficiale on dendrites whose cell bodies appear to be found in the lower part of this layer and in the stratum opticum. The two faster conducting populations synapse deeper, near the border of the stratum griseum superficiale and stratum opticum, on neurons with cell bodies that may lie towards the upper part of the stratum griseum superficiale. The locations of these postsynaptic sites correspond to the layers in which the optic nerve terminates as revealed by neuroanatomical tracing techniques. Furthermore, neurons of the shape and orientation predicted by the current source-density analysis were found in the superficial layers by using the Golgi-Cox technique.     

Amiloride attenuates glycine-induced currents in cultured neurons of rat inferior colliculus

Amiloride, a potassium sparing diuretic, is well known to interact with many ion transport systems and modulate the activity of several membrane receptors. However, relatively little information is available as to how amiloride affects membrane receptors of neurons in the brain areas. In the present study, we investigated the effects of amiloride on glycine-induced currents (I(Gly)) in cultured neurons of rat inferior colliculus with whole-cell patch-clamp recordings. Amiloride itself did not activate any current across the neuronal membrane but it reversibly inhibited the amplitude of the I(Gly) in a reversible and concentration-dependent manner, with an IC(50) of 487.4+/-25.3microM (n=5). Amiloride shifted the concentration-response relationship to the right without changing Hill coefficient and without changing the maximum response of the I(Gly). The pre-perfusion of amiloride produced an inhibitory effect on the I(Gly). In addition, amiloride was shown with a voltage ramp protocol to significantly reduce the conductance induced by glycine but not to change the reversal potential of the I(Gly). These results demonstrate that amiloride competitively inhibits the I(Gly) in rat inferior colliculus neurons by decreasing the affinity of glycine to its receptor. Our finding suggests that attention should be paid to the possible side effects of amiloride used as a drug on brain functions in the case of a defective blood-brain barrier and in the case of direct application of this drug into the cerebrospinal fluid for treatment of brain tumors.     

Distributions of choline acetyltransferase and acetylcholinesterase activities in layers of rat superior colliculus

Choline acetyltransferase (ChAT) and acetylcholinesterase (AChE) activities were assayed in samples dissected from sagittal sections through rat superior colliculus. The magnitude of ChAT activity was about half to equal that found in rat whole brain in all layers except stratum griseum intermediale, where the average activity was higher than whole brain. AChE activity was three to four times that found in rat whole brain in superficial layers and about the same as average brain in deeper layers, except in the statum griseum intermediale, where the average activity was about twice whole brain. Rostral-caudal gradients in both ChAT and AChE activities occurred in stratum griseum intermediale, with activities in the caudal region of some animals as high as four times those in the rostral. ChAT activity in samples associated with locations of patches or spots of AChE staining product in stratum griseum intermediale was significantly higher than in samples from "nonpatch" regions. Results are discussed relative to inputs into the colliculus, whose terminations may correlate in location with the distributions of the enzyme activities.     

Monoamine storage sites in the rat superior cervical ganglion following synthesis inhibition

Summary Monoamine storage sites in paraganglionic (PG-)cells of the rat superior cervical ganglion were investigated by electron and fluorescence microscopy following treatment with p-chlorophenylalanine (pCPA), disulfiram or guanethidine respectively.Dense core vesicles in PG-cells are significantly decreased (p< 0.001) in number following pCPA, and in the majority of these cells following disulfiram and guanethidine. However in a minor portion of PG-cells the latter agents cause an increase in number and in size of dense core vesicles, in parallel with structural alterations. In agreement with these electron microscopic findings fluorescence microscopic and cytophotometric evaluations reveal a general decrease in catecholamine content with few cells showing an increase.The findings provide a morphological basis for the assumption, that monoamine storage sites in PG-cells can be decreased by inhibition of monoamine synthesis, following administration of pCPA, disulfiram and guanethidine. However the two types of responses of PG-cells which occur after disulfiram and guanethidine demonstrate a functional heterogeneity of this cell system in the rat superior cervical ganglion which is discussed.Supported by Deutsche Forschungsgemeinschaft — Grant He 919/1.I like to thank Prof. Arnold, Tübingen, for the kind disposal of cytophotometric equipment.     

Presynaptic dendrite cells and two other classes of neurons in the superficial layers of the superior colliculus of the chimpanzee

In the superior colliculus of chimpanzee, three classes of neurons can be identified by ultrastructural criteria. They are 1) marginal cells located in the stratum zonale, 2) collicular relay cells in the stratum griseum superficiale and 3) presynaptic dendrite (PSD) cells, i.e., neurons with presynaptic specializations in soma and/or dendrites. PSD cells are the smallest neurons in the stratum griseum superficiale; they have a relatively large, deeply infolded nucleus and a small rim of cytoplasm rich in free ribosomes. PSD cells are sufficiently different from the two other classes of neurons to be reliably identified at the ultrastructural level. They closely resemble presynaptic neurons as described in the lateral geniculate nucleus of other mammalian species. Presynaptic dendrites in continuity with PSD cells are rich in organelles, especially ribosomal cluster, and establish en passage contact with other dendrites. Another type of presynaptic dendrite, poor in organelles, except for bundles of microtubules, could not be traced back to its parent neuron. Homo- or heterogeneity of PSD cells is discussed. No amxon was traced from a PSD cell.     

Cellular dispersion patterns and phenotypes in the developing mouse superior colliculus.

The mammalian superior colliculus is structurally and functionally divided into two entities: superficial visual and deep multimodal motor. To discover the role, if any, of developmental processes in establishing separate tectal compartments, we have used highly unbalanced mouse chimaeras to mark cell dispersion pathways and trace cell lineages. Two forms of cell dispersion were detected: radial and tangential. Neither radial nor tangential forms of cell dispersion were found to exist on their own in any group of labeled cells. Radial cell dispersion was the predominant form of cell movement from the germinal zones and primarily associated with the differentiation of glutamatergic neurons. In contrast, tangential cell dispersion involved a minority of tectal cells, concentrated chiefly in the superficial layers and often associated with the upper aspects of radial columns. More scattered cells expressed gamma-aminobutyric acid (GABA) compared to columnar cells. Taken together, these results indicate separate developmental constraints for the development of glutamatergic and GABAergic neurons in the superior colliculus.     

Morphology of calretinin-immunoreactive neurons in the superficial layers of hamster superior colliculus after enucleation: lack of co-localization with GABA

We recently reported on the distribution and effects of eye enucleation on the immunoreactivity of calretinin in the superficial layers of the hamster superior colliculus (SC). In the present study, we describe the types of labeled cells and compare this labeling to that of GABA, the major inhibitory neurotransmitter in the central nervous system. An almost complete depletion of calretinin-immunoreactive (IR) fibers in the superficial layers of the contralateral SC was found following unilateral enucleation. On the contralateral SC, many calretinin-IR cells were newly appeared. The majority of the newly-appeared cells had small- to medium-sized round, oval, or vertical fusiform cell bodies. Two-color immunofluorescence revealed that none of these newly-appeared cells were labeled with an antibody to GABA. The present results show that the calretinin-IR cells are unique in the superficial hamster SC when compared to most of the other brain areas, where many calretinin-IR cells are GABAergic interneurons.     

Mapping visual functions onto molecular cell types in the mouse superior colliculus

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