Diffuse and specific tectopulvinar terminals in the tree shrew: synapses, synapsins, and synaptic potentials. (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, 2006
The lateral posterior (LP) nucleus is a higher order thalamic nucleus that is believed to play a key role in the transmission of visual information between cortical areas. Two types of cortical terminals have been identified in higher order nuclei, large (type II) and smaller (type I), which have been proposed to drive and modulate, respectively, the response properties of thalamic cells Proc. Natl. Acad. Sci. U. S. A. 95:7121-7126). The aim of this study was to assess and compare the relative contribution of driver and modulator inputs to the LP nucleus that originate from the posteromedial part of the lateral suprasylvian cortex (PMLS) and area 17. To achieve this goal, the anterograde tracers biotinylated dextran amine (BDA) or Phaseolus vulgaris leucoagglutinin (PHAL) were injected into area 17 or PMLS. Results indicate that area 17 injections preferentially labelled large terminals, whereas PMLS injections preferentially labelled small terminals. A detailed analysis of PMLS terminal morphology revealed at least four categories of terminals: small type I terminals (57%), medium-sized to large singletons (30%), large terminals in arrangements of intermediate complexity (8%), and large terminals that form arrangements resembling rosettes (5%). Ultrastructural analysis and postembedding immunocytochemical staining for ␥-aminobutyric acid (GABA) distinguished two types of labelled PMLS terminals: small profiles with round vesicles (RS profiles) that contacted mostly non-GABAergic dendrites outside of glomeruli and large profiles with round vesicles (RL profiles) that contacted non-GABAergic dendrites (55%) and GABAergic dendritic terminals (45%) in glomeruli. RL profiles likely include singleton, intermediate, and rosette terminals, although future studies are needed to establish definitively the relationship between light microscopic morphology and ultrastructural features.
Synapsin utilization differs among functional classes of synapses on thalamocortical cells
The Journal of neuroscience : the official journal of the Society for Neuroscience, 2006
Several proteins in nerve terminals participate in synaptic transmission between neurons. The synapsins, which are synaptic vesicleassociated proteins, have widespread distribution in the brain and are assumed essential for sustained recruitment of vesicles during high rates of synaptic transmission. We compared the role of synapsins in two types of glutamatergic synapses on thalamocortical cells in the dorsal lateral geniculate nucleus of mice: retinogeniculate synapses, which transmit primary afferent input at high frequencies and show synaptic depression, and corticogeniculate synapses, which provide modulatory feedback at lower frequencies and show synaptic facilitation. We used electrophysiological methods to determine effects of gene knock-out of synapsin I and II on short-term synaptic plasticity in paired-pulse, pulse-train, and posttetanic potentiation paradigms. The gene inactivation changed the plasticity properties in corticogeniculate, but not in retinogeniculate, synapses. Immunostaining with antibodies against synapsins in wild-type mice demonstrated that neither synapsin I nor II occurred in retinogeniculate terminals, whereas both occurred in corticogeniculate terminals. In GABAergic terminals, only synapsin I occurred. In corticogeniculate terminals of knock-out mice, the density of synaptic vesicles was reduced because of increased terminal size rather than reduced number of vesicles and the intervesicle distance was increased compared with wild-type mice. In the retinogeniculate terminals, no significant morphometric differences occurred between knock-out and wildtype mice. Together, this indicates that synapsin I and II are not present in the retinogeniculate terminals and therefore are not essential for sustained, high-rate synaptic transmission.
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)
Vision Research, 1971
THE MAIN site for transfer of specific information in the nervous system is at the synapse. Among the factors which regulate this transfer process are the transmitter substance at individual synapses and the pattern and position of synapses on postsynaptic structures. It is clear that different regions of the brain contain different amounts of transmitter substances (FAHN and C~TI?, 1968) and have characteristic patterns of synapses not shared by other regions. Little is known, however, as to what directs an axon, not only to end in one specific locus within a region (for example, to maintain a topographical pattern), but also to connect in a highly specific fashion within that locus. Behavioral and physiological studies (e.g. have shown that many basic patterns of connections are laid down independently of the functional organization of extrinsic inputs, exhibiting a so-called "prefunctional" specificity. There are, however, in addition to this rigid framework, indications that further connections and even details of individual synapses can be modified by disturbing function. Thus, have shown that, while the crossed retinotectal map of frog is laid down in an invariant fashion, the "uncrossed" retinotectal map is modifiable by function; have shown that, while maintained eye closure does not affect the topographical map of the retina on the cortex, it does disturb the unitary responses; CRAGG (1969) and have shown in the lateral geniculate body a change in the average size of terminals and in particular synaptic details following maintained eye closure.
Retinohypothalamic Tract Synapses in the Rat Suprachiasmatic Nucleus Demonstrate
The master circadian pacemaker located in the suprachiasmatic nucleus (SCN) is entrained by light intensity-dependent signals transmitted via the retinohypothalamic tract (RHT). Short-term plasticity at glutamatergic RHT-SCN synapses was studied using stimulus frequencies that simulated the firing of light sensitive retinal ganglion cells. The evoked excitatory postsynaptic current (eEPSC) was recorded from SCN neurons located in hypothalamic brain slices. The eEPSC amplitude was stable during 0.08 Hz stimulation and exhibited frequency-dependent shortterm synaptic depression (SD) during 0.5 to 100 Hz stimulus trains in 95 of 99 (96%) recorded neurons. During SD the steady-state eEPSC amplitude decreased, whereas the cumulative charge transfer increased in a frequency-dependent manner and saturated at 20 Hz. SD was similar during subjective day and night and decreased with increasing temperature. Paired-pulse stimulation (PPS) and voltagedependent Ca 2ϩ channel (VDCC) blockers were used to characterize a presynaptic release mechanism. Facilitation was present in 30% and depression in 70% of studied neurons during PPS. Synaptic transmission was reduced by blocking both N-and P/Q-type presynaptic VDCCs, but only the N-type channel blocker significantly relieved SD. Aniracetam inhibited AMPA receptor desensitization but did not alter SD. Thus we concluded that SD is the principal form of short-term plasticity at RHT synapses, which presynaptically and frequency-dependently attenuates light-induced glutamatergic RHT synaptic transmission protecting SCN neurons against excessive excitation.
Synaptic targets of thalamic reticular nucleus terminals in the visual thalamus of the cat
Journal of Comparative Neurology, 2001
A major inhibitory input to the dorsal thalamus arises from neurons in the thalamic reticular nucleus (TRN), which use gamma-aminobutyric acid (GABA) as a neurotransmitter. We examined the synaptic targets of TRN terminals in the visual thalamus, including the A lamina of the dorsal lateral geniculate nucleus (LGN), the medial interlaminar nucleus (MIN), the lateral posterior nucleus (LP), and the pulvinar nucleus (PUL). To identify TRN terminals, we injected biocytin into the visual sector of the TRN to label terminals by anterograde transport. We then used postembedding immunocytochemical staining for GABA to distinguish TRN terminals as biocytin-labeled GABA-positive terminals and to distinguish the postsynaptic targets of TRN terminals as GABA-negative thalamocortical cells or GABA-positive interneurons. We found that, in all nuclei, the TRN provides GABAergic input primarily to thalamocortical relay cells (93-100%). Most of this input seems targeted to peripheral dendrites outside of glomeruli. The TRN does not appear to be a significant source of GABAergic input to interneurons in the visual thalamus. We also examined the synaptic targets of the overall population of GABAergic axon terminals (F1 profiles) within these same regions of the visual thalamus and found that the TRN contacts cannot account for all F1 profiles. In addition to F1 contacts on the dendrites of thalamocortical cells, which presumably include TRN terminals, another population of F1 profiles, most likely interneuron axons, provides input to GABAergic interneuron dendrites. Our results suggest that the TRN terminals are ideally situated to modulate thalamocortical transmission by controlling the response mode of thalamocortical cells. R. 1989. Intrinsic properties of nucleus reticularis thalami neurones of the rat studied in vitro. J Physiol (Lond) 416:111-122. Bal T, McCormick DA. 1993. Mechanisms of oscillatory activity in guineapig nucleus reticularis thalami in vitro: a mammalian pacemaker. J Physiol (Lond) 468:669 -691. Beaulieu C, Cynader M. 1992. Preferential innervation of immunoreactive choline acetyltransferase synapses on relay cells of the cat's lateral geniculate nucleus: a double-labeling study. Neuroscience 47:33-44. Benes FM, Lange N. 2001. Two-dimensional versus three-dimensional cell counting: a practical perspective. Trends Neurosci 24:11-17. Berman N. 1977. Connections of the pretectum in the cat. J Comp Neurol 174:227-254. Berson DM, Graybiel AM. 1978. Parallel thalamic zones in the LP-pulvinar complex of the cat identified by their afferent and efferent connections. Brain Res 147:139 -148. Berson DM, Graybiel AM. 1983. Organization of the striate-recipient zone of the cat's lateralis posterior-pulvinar complex and its relations with the geniculostriate system. Neuroscience 9:337-372. Bickford ME, Gunluk AE, Van Horn SC, Vaughan JW, Godwin DW, Sherman SM. 1994. Thalamic reticular nucleus synaptic targets in the cat LGN. Soc Neurosci Abstr 20:8. Bourassa J, Deschênes M. 1995. Corticothalamic projections from the primary visual cortex in rats: a single fiber study using biocytin as an anterograde tracer. Neuroscience 66:253-263. Carden WB, Bickford ME. 1999. Location of muscarinic type 2 receptors within the synaptic circuitry of the cat visual thalamus. J Comp Neurol 410:431-443. Coleman KA, Mitrofanis J. 1996. Organization of the visual reticular thalamic nucleus of the rat. Eur J Neurosci 8:388 -404. Conley M, Diamond IT. 1990. Organization of the visual sector of the thalamic reticular nucleus in Galago: evidence that the dorsal lateral geniculate and pulvinar nuclei occupy separate parallel tiers. Eur J Neurosci 2:211-226. Conley M, Kupersmith AC, Diamond IT. 1991. The organization of projections from subdivisions of the auditory cortex and thalamus to the auditory sector of the thalamic reticular nucleus in Galago. Eur J Neurosci 3:1089 -1103. Contreras D, Curro Dossi R, Steriade M. 1993. Electrophysiological properties of cat reticular thalamic neurones in vivo. J Physiol (Lond) 470:273-294. Crabtree JW. 1992. The somatotopic organization within the cat's thalamic reticular nucleus. Eur J Neurosci 4:1352-1361. Crabtree JW. 1996. Organization in the somatosensory sector of the cat's thalamic reticular nucleus. J Comp Neurol 366:207-222. Crabtree JW. 1998. Organization in the auditory sector of the cat's thalamic reticular nucleus. J Comp Neurol 390:167-182. Crabtree JW, Killackey HP. 1989. The topographic organization and axis of projection within the visual sector of the rabbit's thalamic reticular nucleus. Eur J Neurosci 1:94 -109. Cucchiaro JB, Uhlrich DJ, Sherman SM. 1991a. Electron-microscopic analysis of synaptic input from the perigeniculate nucleus to the A-laminae of the lateral geniculate nucleus in cats. J Comp Neurol 310:316 -336. Cucchiaro JB, Bickford ME, Sherman SM. 1991b. A GABAergic projection
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.
Journal of comparative neurology, 1991
The perigeniculate nucleus of carnivores is thought to be a part of the thalamic reticular nucleus related to visual centers of the thalamus. Physiological studies show that perigeniculate neurons, which are primarily GABAergic, provide feedback inhibition onto neurons in the lateral geniculate nucleus. However, little is known about the anatomical organization of this feedback pathway. To address this, we used two complementary tracing methods to label perigeniculate axons for electron microscopic study in the geniculate A-laminae: intracellular injection of horseradish peroxidase (HRP) to fill an individual perigeniculate cell and its axon; and anterograde transport of Phaseolus vulgaris leucoagglutinin to label a population of perigeniculate axons. Labeled perigeniculate terminals display features of F1 terminals in the geniculate neuropil: they are small, contain dark mitochondria, and form symmetric synaptic contacts. We found that most of the perigeniculate terminals (> 90%) contact geniculate cell dendrites in regions that also receive a rich innervation from terminals deriving from visual cortex (e.g., "cortico-recipient" dendrites). The remainder of the perigeniculate synapses (10%) contacted dendrites in regions that also received direct retinal input (e.g., "retino-recipient'' dendrites). Serial reconstruction of segments of dendrites postsynaptic to perigeniculate terminals suggests that these terminals contact both classes of relay cell in the A-laminae (X and Y), although our preliminary conclusion is that an individual perigeniculate cell contacts only one class. Finally, our quantitative comparison between labeled perigeniculate terminals and unlabeled F1 terminals indicates that these perigeniculate terminals form a distinct subset of F1 terminals. We quantitatively compared the labeled perigeniculate terminals to unlabeled F1 terminals. Although the parameters of the perigeniculate terminals fell entirely within the range of those for the unlabeled F1 terminals, as populations, we found consistent differences between these two groups. We thus conclude that, as populations, other sources of F1 terminals are morphologically distinct from perigeniculate terminals and innervate different targets.