Quantitative immunogold evidence that glutamate is a neurotransmitter in afferent synaptic terminals within the isthmo-optic nucleus of the pigeon centrifugal visual system (original) (raw)
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Visual Neuroscience, 1995
The present study examined GABA immunoreactivity within the retinopetal nucleus isthmo-opticus (NIO) of the pigeon centrifugal visual system (CVS) using light- (immunohistofluorescence, peroxidase anti-peroxidase: PAP) and electron- (postembedding GABA immunogold) microscopic techniques. In some double-labeling experiments, the retrograde transport of the fluorescent dye rhodamine β−isothiocyanate (RITC) after its intraocular injection was combined with GABA immunohistofluorescence. GABA-immunoreactive (-ir) somata were demonstrated within the neuropilar zone of the NIO adjacent to the centrifugal cell laminae whereas the centrifugal neurons were always immunonegative. A quantitative ultrastructural analysis was performed which distinguished five categories of axon terminal profiles (P1–5) on the basis of various cytological criteria: type of synaptic contact (symmetrical or asymmetrical); shape, size, and density of synaptic vesicles as well as the immunolabeling (positive or negat...
The Journal of Comparative Neurology, 2008
The ultrastructure of the lateroventral subcomponent of the visual dorsolateral anterior thalamic nucleus of the pigeon (DLLv) was analyzed using hodological techniques and GABA-immunocytochemistry. Two types of GABA-immunonegative hyperpalliopetal neurons and a single type of strongly GABA-immunoreactive (-ir) interneuron were identified, the latter displaying long dendrites with some containing synaptic vesicles (DCSV). Ten types of axon terminal were identified and divided into two categories. The first, GABAimmunonegative and making asymmetrical synaptic contact, contain round (RT1, RT2, RT3) or pleiomorphic synaptic and many dense-core vesicles (DCT). RT1 terminals are retinothalamic and RT2 terminals hyperpalliothalamic; both mainly contact dendrites of projection neurons (72% and 78% respectively), less frequently dendrites of interneurons and sometimes DCSV; RT1 terminals are rarely involved in synaptic triads. The second category are consistently GABA-immunopositive. Four types (PT1-4), distinguished by their pleiomorphic synaptic vesicles, make symmetrical synaptic contact essentially with dendrites of projection neurons, more rarely on dendrites of interneurons (PT2). PT1 terminals are very probably those of interneurons, whereas the rare PT4 terminals are of retinal origin. A fifth type (RgT) contains round synaptic vesicles and makes asymmetrical synaptic contact with dendrites of projection neurons and interneurons. PT2 and RgT terminals occasionally contact DCSV of interneurons, which are sometimes involved in synaptic triads. Two final subcategories (DCgT1-2) contain many dense-core vesicles. Our findings are compared with those of previous studies concerning the fine structure and neurochemical properties of the GLd of reptiles and mammals, with special reference to the origin of the extraretinal and extracortical projections to this structure.
Journal of Comparative Neurology, 2014
The nucleus geniculatus lateralis pars ventralis (GLv) is a prominent retinal target in all amniotes. In birds, it is in receipt of a dense and topographically organized retinal projection. The GLv is also the target of substantial and topographically organized projections from the optic tectum and the visual wulst (hyperpallium). Tectal and retinal afferents terminate homotopically within the external GLvneuropil. Efferents from the GLv follow a descending course through the tegmentum and can be traced into the medial pontine nucleus. At present, the cells of origin of the Tecto-GLv projection are only partially described. Here we characterized the laminar location, morphology, projection pattern, and neurochemical identity of these cells by means of neural tracer injections and intracellular fillings in slice preparations and extracellular tracer injections in vivo. The Tecto-GLv projection arises from a distinct subset of layer 10 bipolar neurons, whose apical dendrites show a complex transverse arborization at the level of layer 7. Axons of these bipolar cells arise from the apical dendrites and follow a course through the optic tract to finally form very fine and restricted terminal endings inside the GLv-neuropil. Double-label experiments showed that these bipolar cells were choline acetyltransferase (ChAT)immunoreactive. Our results strongly suggest that Tecto-GLv neurons form a pathway by which integrated tectal activity rapidly feeds back to the GLv and exerts a focal cholinergic modulation of incoming retinal inputs.
Journal of Chemical Neuroanatomy, 1998
The aim of the present study was to analyze the neurochemical properties of the centrifugal visual system (CVS) of the quail using an immunohistochemical approach by testing 16 neuropeptides (angiotensin: ANG, bradykinin: BK, cholecystokinin, dynorphin, L and M-enkephalin, i-endorphin: i-END, galanin, h-neoendorphin, neurokinin A, neuropeptide Y (NPY), ocytocin, somatostatin, substance P, vasopressin, vasoactive intestinal polypeptide) and three neurotransmitters or their synthetic enzymes (choline acetyltransferase: ChAT, tyrosine hydroxylase: TH, serotonin: 5-HT and nitric oxide synthase: NOS, including the histochemical nicotinamide adenine dinucleotide phosphate diaphorase technique). For each substance, the somatic and afferent fiber and terminal labeling was analyzed within the nucleus isthmo-opticus (NIO) and the ectopic area (EA) and compared with that of retinopetal cell bodies labeled retrogradely with RITC following its intraocular injection (double-labeling procedure). The results showed that none of the centrifugal neurons were reactive to any of the substances tested. In contrast, all with the exception of ANG, BK and i-END, labeled fibers and terminals within the EA and only four (ChAT, 5-HT, NPY and NOS) within the NIO. Possible sources of these immunoreactive fibers terminating in the NIO and EA were investigated by mapping the somatic immunolabeling of the different substances within brainstem regions previously shown by Miceli and other authors to project upon the centrifugal neurons. The data suggests that, besides the rapid retino-tecto-NIO-retinal loop, which facilitates the transfer of meaningful or more relevant information within particular portions of the visual field, the multiple afferent input which stems from various brainstem regions utilizes a wide range of neuroactive substances. Some of these afferent projections upon the centrifugal neurons appear to belong to nonspecific systems which might play a role in modulating the Abbre6iations: AL, ansa lenticularis; AVT, area ventralis of TSAI; Cb, cerebellum; Ce, externel laminae of the nucleus isthmo-opticus; Ci, internel laminae of the nucleus isthmo-opticus; Cp, commissura posterior; EA, ectopic area; EC, centrifugal ectopic neurons; EW, nucleus of Edinger-Westphal; FLM, fasciculus longitudinalis medialis; FRL, formatio reticularis lateralis mesencephali; FRM, formatio reticularis lateralis mesencephali; ICo, nucleus intercollicularis; Imc, nucleus isthmi magnocellularis; Ipc, nucleus isthmi parvocellularis; L7, 9 -10, layers 7, 9 -10 of the optic tectum; LC, nucleus linearis caudalis; Li, lingula; LoC, nucleus ceruleus; MLd, nucleus mesencephalicus pars dorsalis; N, neuropilar zone of the nucleus isthmo-opticus; N III, nervus oculomotorius; N IV, nucleus nervis trochlearis; NV, nervus trigeminus; N VII, nucleus nervi facialis; N VIII, nervus octatus; N IX, nucleus nervi glossopharyngei; nBOR, nucleus of the basal optic root; NIO, nucleus isthmo- 00034-9 M. Médina et al. / Journal of Chemical Neuroanatomy 72 (1998) 75-95 76 excitability of centrifugal neurons as a function of arousal.
The Journal of Comparative Neurology, 1997
The tectofugal pathway is a massive ascending polysynaptic pathway from the tectum to the thalamus and then to the telencephalon. In birds, the initial component of this pathway is known as the tectorotundal pathway; in mammals, it is known as the tectopulvinar pathway. The avian tectorotundal pathway is highly developed; thus, it provides a particularly appropriate model for exploring the fundamental properties of this system in all amniotes. To further define the connectivity of the tectorotundal projections of the tectofugal pathway, we injected cholera toxin B fragment into various rotundal divisions, the tectobulbar projection, and the ventral supraoptic decussation of the pigeon. We found intense bilateral retrograde labeling of neurons that stratified within layer 13 and, in certain cases, granular staining in layer 5b of the optic tectum. Based on these results, we propose that there are two distinct types of layer 13 neurons that project to the rotundus: 1) type I neurons, which are found in the outer sublamina of layer 13 (closer to layer 12) and which project to the anterior and centralis rotundal divisions, and 2) type II neurons, which are found in the inner sublamina of layer 13 (closer to layer 14) and which project to the posterior and triangularis rotundal divisions. Only the labeling of type I neurons produced the granular dendritic staining in layer 5b. An additional type of tectal neuron was also found that projected to the tectobulbar system. We then injected Phaseolus vulgaris-leucoagglutinin in the optic tract and found that the retinal axons terminating within tectal layer 5b formed narrow radial arbors (7-10 µm in diameter) that were confined to layer 5b. Based on these results, we propose that these axons are derived from a population of small retinal ganglion cells (4.5-6.0 µm in diameter) that terminate on the distal dendrites of type I neurons.
The Journal of Comparative Neurology, 1991
Retrograde transport of Phaseolus uulgaris leucoagglutinin (PHA-L), fluorogold, fast blue, rhodamine labelled microspheres, and horseradish peroxidase (HRP) was employed to study the distribution, laminar location within the optic tectum, and morphology of tectal cells projecting upon the isthmo-optic nucleus (ION) and the nucleus isthmi, pars parvocellularis (Ipc), in the pigeon and chick. Following injections into the ION, all retrograde markers labelled tecto-ION neurons and their dendrites in the ipsilateral tectum. The cells were located within a relatively narrow band at the border between layers 9 and 10 of the stratum griseum et fibrosum superficiale (SGFS). Retrogradely labelled neuronal somata were different in both dendritic branching and shape; however, tecto-ION neurons generally possessed non-spiny radially oriented and multibranched dendrites. The apical processes extended into the retino-recipient layers (2-7) of the SGFS and basal dendrites extended into layers 12-14 of the SGFS. Positive neuronal somata were observed throughout the rostro-caudal extent of the optic tectum. The average distance between adjacent tecto-ION neurons varied from one region to another. Specifically, retrogradely labelled cells were more numerous in the caudal, lateral, and ventral tectum, and less numerous at rostro-dorsal levels. Approximately 12,000 tecto-ION neurons were labelled within the ipsilateral optic tectum following either PHA-L or fluorescent dye injections. While the regional distribution of tecto-Ipc neurons was not examined, the morphology indicated that the cells had a single radially oriented dendritic process. Therefore, the apical dendrites are more restricted than those of tecto-ION cells. Moreover, the dendrites were spiny and arborized within layers 3,5, and 9 of the ipsilateral optic tectum. The axon of tecto-Ipc cells arise from the apical process as a shepherd's crook and descend into the deep layers of the optic tectum. These results indicate that 1) tecto-ION and tecto-Ipc neurons are possibly monosynaptically activated by retinal input, 2) tecto-ION neurons are heterogeneous in morphology, and 3) there is a differential distribution of the tecto-ION neurons throughout the rostro-caudal extent of the optic tectum, suggesting a greater representation of the caudo-ventral portion of the optic tectum within the ION. The discussion primarily concerns the organization of the retino-tecto-ION-retinal circuit in light of the distribution and morphology of tecto-ION neurons within the optic tectum.
The Journal of Comparative Neurology, 1985
The responses of 65 cells to electrical stimulation of the contralateral optic nerve were intracellularly recorded in the pigeon optic tectum by using micropipettes filled with a solution of horseradish peroxidase. Nineteen of them were successfully labeled. Microscopic examination of the filled cells shows that our sample includes six pyramidal, ten ganglion, two stellate, and one bipolar horizontal cells. Thus, pyramidal and ganglion neurons constitute the most numerous types of cells in our sample. Pyramidal cells were located in layer I1 but mostly in its non-retinorecipient part, and they had restricted ascending dendritic trees oriented orthogonal to the tectal lamination. Ganglion cells were located in layer 1 1 1 with one exception, which was in sublayer IIi. These cells had non-oriented dendritic trees which ramify over considerable distances. Terminal dendritic branches from a number of pyramidal and ganglion cells extended superficially well within the region of optic fibers termination. In our study, ganglion cells constituted the efferent tectal elements. Pyramidal cells responded to optic nerve stimulation with a pure EPSP, with an EPSP-IPSP sequence, or with a pure IPSP. Ganglion cells always exhibited an IPSP either alone or preceded by an EPSP. Stellate and bipolar cells responded with a pure EPSP. The study of the laminar distribution of labeled and non-labeled cells shows from surface to depth, a gradual increase in the number of cells responding with an EPSP-IPSP or with a pure IPSP and a gradual decrease in the number of those exhibiting a pure EPSP. The analysis of the sensitivity of EPSPs and IPSPs to high frequency optic nerve stimulation shows that 1) monosynaptic as well as polysynaptic EPSPs can be recorded from cells in the non-retinorecipient tectal region, 2) a number of ganglion and pyramidal cells receive a direct retinal excitatory input as their dendrites pass through the region of optic endings, 3) most IPSPs are polysynaptic, 4) some cells located in the retinorecipient region may receive direct retinal inhibitory connections.
European Journal of Neuroscience, 2000
The optic tectum of the pigeon is a highly organized, multilayered structure that receives a massive polystratified afference of at least five different populations of retinal ganglion cells and gives rise to various anatomically segregated efferent systems. The synaptic organization of retino-tectal circuitry is, at present, mostly unknown. To investigate the spatiotemporal profile of synaptic activation produced by differential (electrical and visual) stimulation of the retinal inputs, we performed a high-spatial-resolution current source density analysis in the optic tectum of the anaesthetized pigeon. Electrical stimuli consisted of brief pulses of different durations applied to the optic nerve head, while visual stimuli consisted of light flashes of different intensities. Electrical stimulation generated sinks confined to retinorecipient layers. The temporal structure, spatial location and thresholds of these sinks indicated that they are all due to primary tectal synapses of retinal fibers with different conduction velocities. Sinks evoked by the fastest retinal axons were more superficially located than sinks produced by slower retinal fibers. Visual stimulation, on the other hand, resulted in a more complex pattern of current sinks, with various sinks located in the retinorecipient layers and also well below. Visual stimulation induced action potentials at superficial as well as deep tectal levels. We conclude that electrical stimulation activates most of the populations of ganglion cells as well as their primary tectal synapses, but is unable to elicit a significant activation of secondary tectal synapses. Visual stimulation, on the contrary, activates just some of the incoming retinal populations, but in a way that produces noticeable secondary activation of intratectal circuits. Laminar segregation of retinally evoked tectal activity, as reported here, has also been found in other vertebrates. Similarities and differences with previous studies are discussed.