Electron-microscopic analysis of synaptic input from the perigeniculate nucleus to the A-laminae of the lateral geniculate nucleus in cats (original) (raw)
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Relative distribution of synapses in the A-laminae of the lateral geniculate nucleus of the cat
Journal of Comparative Neurology, 2000
Previous electron microscopic studies of synaptic terminal distributions in the lateral geniculate nucleus have been flawed by potential sampling biases favoring larger synapses. We have thus re-investigated this in the geniculate A-laminae of the cat with an algorithm to correct this sampling bias. We used serial reconstructions with the electron microscope to determine the size of each terminal and synaptic type. We observed that RL (retinal) terminals are largest, F (local, GABAergic, inhibitory) terminals are intermediate in size, and RS (cortical and brainstem) terminals are smallest. We also found that synapses from RL terminals are largest, and thus most oversampled, and we used synaptic size data to correct for sampling errors. Doing so, we found that the relative synaptic percentages overall are 11.7% for RL terminals, 27.5% for F, and 60.8% for RS. Furthermore, we distinguished between relay cells and interneurons with post-embedding immunocytochemistry for GABA (relay cells are GABA negative and interneurons are GABA positive). Onto relay cells, RL terminals contributed 7.1%, F terminals contributed 30.9%, and RS terminals contributed 62.0%. Onto interneurons, RL terminals contributed 48.7%, F terminals contributed 24.4%, and RS terminals contributed 26.9%. We also found that RL terminals included many more separate synaptic contact zones (9.1 Ϯ 1.6) than did F terminals (2.6 Ϯ 0.2) or RS terminals (1.02 Ϯ 0.02). We used these data plus the calculation of overall percentages of each synaptic type to compute the relative percentage of each terminal type in the neuropil: RL terminals represent 1.8%, F terminals represent 14.5%, and RS terminals represent 83.7%. We argue that this relative synaptic paucity is typical for driver inputs (from retina), whereas modulator inputs (all others) require many more synapses to achieve their function.
The Journal of Comparative Neurology, 1993
We have recently shown in cats that many neurons projecting to the lateral geniculate nucleus from the pretectum use y-amino butyric acid (GABA) as their neurotransmitter. We sought to determine the morphology of synaptic terminals and synapses formed by these pretectal axons and the extent to which they resemble other GAI3Aergic terminals found in the geniculate neuropil (i.e., from geniculate interneurons and cells of the nearby perigeniculate nucleus). To do this, we labeled a population of pretectal axons with the anterograde tracer Phaseolus vulgaris leucoagglutinin and analyzed the morphology and synaptology of labeled pretectal terminals in the A-laminae of the cat's lateral geniculate nucleus. The pretectal projection, which arises primarily from the nucleus of the optic tract (NOT), provides synaptic innervation to elements in the geniculate neuropil. The labeled NOT terminals are densely packed with vesicles, contain dark mitochondria, and form symmetrical synaptic contacts. These are characteristics of the F1 type of terminal, and we know from other studies that GABAergic axon terminals from interneurons and perigeniculate cells also give rise to F1 terminals. We compared our population of NOT terminals with labeled perigeniculate and unlabeled F1 terminals selected from the geniculate neuropil and found that all three populations share many morphological characteristics. Both qualitative and quantitative assessments of the pretectal terminals suggest that these are a type of F1 terminal. Most pretectal terminals selectively form synapses onto geniculate profiles that contain irregularly distributed vesicles and dark mitochondria and that are postsynaptic to other types of terminals. These postsynaptic targets thus exhibit features of another class of inhibitory, GABAergic terminal known as F2 terminals, which are the specialized appendages of geniculate interneurons. Pretectal inputs, being GABAergic, may thus serve to inhibit local interneuronal outputs. Pretectal axons also innervate the perigeniculate nucleus, in which the only targets are the other main type of inhibitory, GABAergic neurons. These results suggest that the pretectum may facilitate retinal transmission through the lateral geniculate nucleus by providing inhibition to the local inhibitory cells: the interneurons and probably perigeniculate cells. This would serve to release geniculate relay cells from inhibition.
Journal of Comparative Neurology, 1998
Laminae A and A1 of the lateral geniculate nucleus in the cat are generally considered to be a structurally and functionally matched pair of inputs from two eyes, although there are subtle light microscopic and physiological differences. The present study aims to display ultrastructural differences between these two laminae based on electron microscopic observances on the connectivity patterns of their afferents onto two main cell types: relay cells, and interneurons present in this nucleus. In a design of population measurement from randomized sample areas in laminae A and A1 from six brains, all synaptic contacts made by three terminal types of the geniculate nucleus were identified, and a number of relative distribution properties were analyzed. When the A-laminae were considered as a homogeneous structure, the distribution of the three terminal types on geniculate cells was similar to previously reported results, confirming the validity of the sampling strategies used; RLP (retinal) terminals provided one-fifth of all synapses, whereas RD (from cortex and brainstem) and F (inhibitory) types constituted one-half and one-third, respectively. The relay cells alone received a similar composition of afferents. However, interneurons alone received approximately equal amounts of synapses from the three sources. Similar analyses comparing the distributions in lamina A and A1 revealed that RD and F terminals, but not RLP terminals, innervate these two laminae differently; more RD and fewer F terminals were found in lamina A1. This difference was also present in the distribution of terminals on relay cells alone, but not on interneurons. These results suggest that (1) retinal terminals form a significantly larger fraction of the input to interneurons than to relay cells; correspondingly, cortex and brainstem provide a smaller fraction of all inputs to interneurons than to relay cells; and (2) laminae A and A1 are not strictly equivalent projection sites of the two retinae. The results are discussed in relation to the Y-cell subpopulation in lamina A1 that is involved in corticotectal, as well as corticogeniculate circuits, as opposed to Y-cells of lamina A that are involved in only the latter.
Dendritic current flow in relay cells and interneurons of the cat's lateral geniculate nucleus
Proceedings of the National Academy of Sciences, 1989
We used a passive, steady-state cable model to simulate current flow within the dendritic arbors of relay cells and interneurons in the cat's lateral geniculate nucleus. In confirmation of our previous work on relay cells, we found them to be electrotonically compact; thus a postsynaptic potential generated anywhere in a relay cell's dendritic arbor spreads with relatively little attenuation throughout the arbor and to its soma. An interneuron is very different. Its arbor is much more extensive electrotonically with the result that a postsynaptic potential significantly affects only local areas of the dendritic arbor, and only inputs to proximal dendrites or to the soma will much affect the soma. Since much of the interneuron's synaptic output derives from dendritic terminals that are both presynaptic and postsynaptic, its dendritic arbor may contain many local circuits that perform neuronal computations independently of each other, and this processing might be invisible to the soma. Furthermore, these interneurons possess conventional axonal outputs, and these contact postsynaptic profiles that are quite different from the postsynaptic targets of the dendritic terminals. Presumably, the axonal output reflects the integrated computations performed on proximal synaptic inputs, and it uses conventional action potentials to convey this output. We suggest that the interneuron does double duty: its dendritic arbor is used for many independent local circuits that perform one set of neuronal computations, and its axonal output represents conventional neuronal integration of proximal synaptic inputs.
Morphology and axonal projection patterns of individual neurons in the cat perigeniculate nucleus
Journal of neurophysiology, 1991
1. The lateral geniculate nucleus is the primary thalamic relay through which retinal signals pass en route to cortex. This relay is gated and can be suppressed by activity among local inhibitory neurons that use gamma-aminobutyric acid (GABA) as a neurotransmitter. In the cat, a major source of this GABAergic inhibition seems to arise from cells of the perigeniculate nucleus, which lies just dorsal to the A-laminae of the lateral geniculate nucleus. However, the morphological characteristics of perigeniculate cells, and particularly the projection patterns of their axons, have never been fully characterized. We thus examined the morphology of these cells: individually by intracellular injection of horseradish peroxidase (HRP) and en masse with the anterograde tracer Phaseolus vulgaris leucoagglutinin (PHAL). 2. We recorded from 12 perigeniculate cells that we impaled and successfully labeled with HRP. These cells exhibited response properties generally consistent with those describ...
Synaptology of retinal terminals in the dorsal lateral geniculate nucleus of the cat
The Journal of Comparative Neurology, 1984
We have made a fine structural investigation of the synaptic patterns made by axon terminals of retinal ganglion cells in the dorsal lateral geniculate nucleus of the cat. We compared the retinal input to dendritic processes that bear clusters of large appendages with the retinal input to relatively smooth dendritic segments that have only a few isolated spines. The study was restricted to the portion of laminae A and A1 that receive central visual field input. We were able to completely reconstruct 33 individual terminal boutons from long series of consecutive thin sections. Retinal terminals that were presynaptic to dendritic appendages tended to occupy the central position in the complex synaptic zones of geniculate fine structure called glomeruli. These terminals were surrounded by significantly more profiles than retinal terminals that were presynaptic to dendritic stems and averaged twice as many synaptic contacts per terminal bouton. The retinal input to dendritic appendages was heavily involved in a specific synaptic pattern called the triadic arrangement while retinal input to dendritic stems was only lightly involved in triads. Dendritic appendages in triads received greater synaptic input from profiles with flattened vesicles than did the dendritic stems that were found in triads.
Synaptic circuits involving an individual retinogeniculate axon in the cat
The Journal of Comparative Neurology, 1987
In order to describe the circuitry of a single retinal X-cell axon in the lateral geniculate nucleus, we physiologically characterized such an axon in the optic tract and injected it intra-axonally with horseradish peroxidase. Subsequently, we recovered the axon and employed electron microscopic techniques to examine the distribution of synapses from 18% of its labeled terminals by reconstructing the unlabeled postsynaptic neurons through a series of 1,200 consecutive thin sections. We found remarkable selectivity for the axon's output, since only four of the 43 available neurons in a limited portion of the terminal arbor receive synapses from labeled terminals. Moreover, the distribution of these synapses on the four neurons, which we term cells 1 through 4 , varies with respect to synapses from other classes of terminals that contact the same cells, including synapses from unlabeled retinal terminals. For cells 1 and 3, the labeled terminals provide 49% and 33%, respectively, of their retinal synapses, and these are located on both dendritic shafts and appendages. Synapses from the injected axon to these cells are thus integrated with those from other retinal axons. For cell 2, the labeled terminals provide 100% of its retinal synapses, but these synapses converge on clusters of dendritic appendages where they are integrated with convergent inhibitory inputs. Finally, for cell 4 , the labeled terminals provide less than 2% of its retinal inputs, and these are distally located; we suggest that these synapses are remnants of physiologically inappropriate miswiring that occurs during development. The findings from this study support a concept of selectivity in neuronal circuitry in the mammalian central nervous system and also reveal some of the diverse integrative properties of neurons in the lateral geniculate nucleus. Laminae A and A1 of the cat's lateral geniculate nucleus identify (Peters and Palay, '66; Guillery, '69a,b; Famiglietti represent a useful model system for studying the neuroan-and Peters, '72; Szentagothai, '73; Robson and Mason, '79). atomical basis of sensory neural processing (Guillery, '69a,b; Finally, recent studies have examined some of the differ-Famiglietti and Peters, '72; LeVay and Ferster, '77; Singer, ences in the synaptology of geniculate Xand Y-cells (Ma-'77; Friedlander et al., '81; Fitzpatrick et al., '84; Wilson et son et al., '84; Wilson et al., '84; Hamos et al., '85; Van al., '84). Much attention has been focused on the parallel X-Horn et al., '85)
The Journal of Comparative Neurology, 1985
Specific thalamic afferents to visual areas 17 and 18 were physiologically classified as X or Y type and injected with horseradish peroxidase (HRP). The axons were examined under the light microscope and were then processed for correlated electron microsocpy. X axons arborised in area 17 and in the border between area 17 and 18. The X axons all formed terminals throughout layer 6, but were heterogeneous in their distribution in layer 4. They either occupied the entire width of sublayers 4A and 4B or were strongly biased toward layer 4A. Y axons also arborised in layers 4 and 6, but in area 17 they did not form boutons in sublamina 4B. Some Y axons projected only to area 18; others branched and arborised in both areas 17 and 18. Only the collaterals of one X axon were found to enter area 18; all the others were restricted to area 17. Y axons formed three to four separate patches of boutons about 300-400 pm in diameter, while all but one X axon formed a single elongated patch. Y axons had thicker main branches (3-4 pm) than X axons (1.5-2.5 pm) at their point of entry to the cortex. The main axon trunks and their medium-calibre collaterals were myelinated, but the preterminal segments were unmyelinated and studded with boutons. Each X or Y axon contacted about seven to ten somata, but Y axons made more contacts per soma (three to six) than did X axons (two to three). In addition to somatic synapses, both X and Y axons formed asymmetric (type 1) synapses on dendritic spines and shafts, with spines forming the most frequent targets (80%). Each Y bouton made, on average, 1.64 synapses in area 17 and 1.79 synapses in area 18, whereas each X bouton made only 1.27 synapses on average. Although there are proportionally fewer Y axons than X axons entering area 17, the Y axons provide as many synapses as the X axons because of their larger arbors and multisynaptic boutons.