A quantitative study of synaptic contacts on interneurons and relay cells of the cat lateral geniculate nucleus
Tóm tắt
The relative proportions of synapses made by retinal and extraretinal terminals on interneurons and relay cells in lamina A of the dorsal lateral geniculate nucleus (LGN) of the cat were estimated quantitatively in a sample of 4003 synapses. Processes of interneurons or relay cells were identified by presence or absence of GABA immunoreactivity, respectively, in thin sections treated with post-embedding anti-GABA immunogold. On the basis of ultrastructural features, synaptic terminals were interpreted as belonging to retinal axons, cortical axons or axon collaterals of relay cells. GABAergic terminals were positively identified by being immunoreactive. GABA(-) terminals with heterogeneous and poorly defined characteristics, which could not be identified in the above classes, were grouped together in an “undetermined” category. Among the total synaptic inputs to interneurons, the following relative percentages of synapses from different terminals were obtained: retinal 25%, cortical 37%, GABAergic 26%, axon collaterals 2%, undetermined 6%. The vast majority of retinal terminals synapse on dendritic appendages of interneurons rather than on their dendritic trunks (about 20∶1). By contrast, the majority of cortical terminals synapse on dendrites rather than on dendritic appendages (about 5∶1). Virtually all axon-collaterals synapses were established on dendritic appendages. 17% of the dendritic profiles of interneurons contain synaptic vesicles; many of these profiles were seen in postsynaptic relation to cortical axons and in presynaptic relation with relay dendrites. Given the extensive electrotonic lengths of these cells observed by others, and the expected high electric resistance of the slender stalks that are known to connect the dendritic appendages to interneurons, these results suggest that microcircuits involving the interneuronal dendritic appendages with dendrites of relay cells are under predominantly retinal control. The microcircuits established by presynaptic dendritic trunks with relay dendrites, are under predominantly cortical control. The axonal (spiking) output of interneurons would be under control of the few retinal synapses on proximal dendrites of these cells. Among the total synaptic inputs to relay cells, the following relative percentages of different synapses were obtained: retinal 12%, cortical 58%, GABAergic 24%, axon collaterals 0.3%, undetermined 5%. Relay cells receive twice the number of cortical synapses than interneurons, suggesting that direct cortical excitatory influences on relay cells are more preponderant than cortico-interneuron mediated inhibition on these cells. The observed proportions of dendritic profiles of relay cells and interneurons (80% and 20%, respectively) in the geniculate neuropil are similar to the known proportions of somata of both types of cells in the A-laminae. This suggests a similarity in the average dendritic branching of relay cells and interneurons.
Tài liệu tham khảo
Ahlsén G, Lindström S (1983) Corticofugal projection to perigeniculate neurons in the cat. Acta Physiol Scand 118:181–184
Ahlsén G, Lindström S, Lo FS (1985) Interaction between inhibitory pathways to principal cells in the lateral geniculate nucleus of the cat. Exp Brain Res 58:134–143
Bloomfield SA, Sherman SM (1989) Dendritic current flow in relay cells and interneurons of the cat's lateral geniculate nucleus. Proc Natl Acad Sci USA 86:3911–3914
Cucchiaro JB, Uhlrich DJ, Hamos JE, Sherman SM (1985) Perigeniculate input to the cat's lateral geniculate nucleus: A light and electron microscopic study of single, HRP-filled cells. Soc Neurosci Abstr 11:231
de Lima AD, Singer W (1987a) The serotonergic fibers in the dorsal lateral geniculate nucleus of the cat: distribution and synaptic connections demonstrated with immunocytochemistry. J Comp Neurol 258:339–351
de Lima AD, Singer W (1987b) The brainstem projection to the lateral geniculate nucleus in the cat: identification of cholinergic and monoaminergic elements. J Comp Neurol 259:92–121
de Lima AD, Montero VM, Singer W (1985) The cholinergic innervation of the visual thalamus. Exp Brain Res 59:206–212
Dubin MW, Cleland BG (1977) Organization of visual inputs to interneurons of lateral geniculate nucleus of the cat. J Neurophysiol 40:410–427
Famiglietti EVJ (1970) Dendro-dendritic synapses in the lateral geniculate nucleus of the cat. Brain Res 20:181–191
Famiglietti EVJ, Peters A (1972) The synaptic glomerulus and the intrinsic neuron in the dorsal lateral geniculate nucleus of the cat. J Comp Neurol 144:285–334
Fitzpatrick D, Penny GR, Schmechel DE (1984) Glutamic acid decarboxylase-immunoreactive neurons and terminals in the lateral geniculate nucleus of the cat. J Neurosci 4:1809–1829
Fitzpatrick D, Diamond IT, Raczkowski D (1989) Cholinergic and monoaminergic innervation of the cat's thalamus: comparison of the lateral geniculate nucleus with other principal sensory nuclei. J Comp Neurol 288:647–675
Francesconi W, Müller CM, Singer W (1988) Cholinergic mechanisms in the reticular control of transmission in the cat lateral geniculate nucleus. J Neurophys 59:1690–1718
Geisert EE (1980) Cortical projections of the lateral geniculate nucleus in the cat. J Comp Neurol 190:793–812
Guillery RW (1966) A study of Golgi preparations from the dorsal lateral geniculate nucleus of the adult cat. J Comp Neurol 128:21–50
Guillery RW (1969a) The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat. Z Zellforsch 96:1–38
Guillery RW (1969b) A quantitative study of synaptic interconnections in the dorsal lateral geniculate nucleus of the cat. Z Zellforsch 96:39–48
Hamos JE, Van Horn SC, Raczkowski D, Uhlrich DJ, Sherman SM (1985) Synaptic connectivity of a local circuit neurone in lateral geniculate nucleus of the cat. Nature 317:618–621
Harvey AR (1980) A physiological analysis of subcortical and commissural projections of areas 17 and 18 in the cat. J Physiol 302:507–534
Holdefer RN, Norton TT, Mize RR (1988) Laminar organization and ultrastructure of GABA-immunoreactive neurons and processes in the dorsal lateral geniculate nucleus of the tree shrew (Tupaia belangeri) Visual Neurosci 1988:189–204
Ide LS (1982) The fine structure of the perigeniculate nucleus in the cat. J Comp Neurol 210:317–334
Le Vay S, Ferster D (1979) Proportion of interneurons in the cat's lateral geniculate nucleus. Brain Res 164:304–308
Lindström S (1983) Interneurons in the lateral geniculate nucleus with monosynaptic excitation from retinal ganglion cells. Acta Physiol Scand 119:101–103
Lindström S, Wróbel A (1990) Private inhibitory systems for the X and Y pathways in the dorsal lateral geniculate nucleus of the cat. J Physiol (London) 429:259–280
Livingstone MS, Hubel DH (1981) Effects of sleep and arousal on the processing of visual information in the cat. Nature 291:554–561
Mason CA, Guillery RW, Rosner MC (1984) Patterns of synaptic contact upon individually labeled large cells of the dorsal lateral geniculate nucleus of the cat. Neuroscience 11:319–329
McCormick DA (1989) Cholinergic and noradrenergic modulation of thalamocortical processing. Trends Neurosci 12:215–221
McCormick DA, Pape HC (1988) Acetylcholine inhibits identified interneurons in the cat lateral geniculate nucleus. Nature 334:246–248
Montero VM (1986) Localization of gamma-aminobutyric acid (GABA) in type 3 cells and demonstration of their source to F2 terminals in the cat lateral geniculate nucleus: a Golgi-electronmicroscopic GABA-immunocytochemical study. J Comp Neurol 254:228–245
Montero VM (1987) Ultrastructural identification of synaptic terminals from the axon of type 3 interneurons in the cat lateral geniculate nucleus. J Comp Neurol 264:268–283
Montero VM (1989a) The GABA-immunoreactive neurons in the interlaminar regions of the cat lateral geniculate nucleus: light and electron microscopic observations. Exp Brain Res 75:497–512
Montero VM (1989b) Ultrastructural identification of synaptic terminals from cortical axons and from collateral axons of geniculo-cortical relay cells in the perigeniculate nucleus of the cat. Exp Brain Res 75:65–72
Montero VM (1990) Quantitative immunogold analysis reveals high glutamate levels in synaptic terminals of retino-geniculate, cortico-geniculate, and geniculo-cortical axons in the cat. Visual Neurosci 4:437–443
Montero VM, Robles L (1971) Saccadic modulation of cell discharges in the lateral geniculate nucleus. Vision Res 11 (Suppl 3):253–268
Montero VM, Scott GL (1981) Synaptic terminals in the dorsal lateral geniculate nucleus from neurons of the thalamic reticular nucleus: A light and electron microscope autoradiographic study. Neuroscience 6:2561–2577
Montero VM, Singer W (1984) Ultrastructure and synaptic relations of neural elements containing glutamic acid decarboxylase (GAD) in the perigeniculate nucleus of the cat: a light and electron microscopic immunocytochemical study. Exp Brain Res 56:115–125
Montero VM, Singer W (1985) Ultrastructural identification of somata and neural processes immunoreactive to antibodies against glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the cat. Exp Brain Res 59:151–165
Montero VM, Wenthold R (1989) Quantitative immunogold analysis reveals high glutamate levels in retinal and cortical synaptic terminals in the lateral geniculate nucleus of the macaque. Neuroscience 31:634–647
Montero VM, Zempel J (1985) Evidence for two types of GABA-containing interneurons in the A-laminae of the cat lateral geniculate nucleus: a double-label HRP and GABA-immunocytochemical study. Exp Brain Res 60:603–609
Murphy PC, Sillito AM (1987) Corticofugal feedback influences the generation of length tuning in the visual pathway. Nature 329:727–729
Ottersen OP (1989) Quantitative electron microscopic immunocytochemistry of neuroactive amino acids. Anat Embryol 180:1–15
Paré D, Curro Dossi R, Steriade M (1990) Genesis of inhibitory postsynaptic potentials (IPSPs) by interneurons in the feline anterior thalamic (AT) nuclei. Soc Neurosci Abstr 16:467
Peters A, Palay SL, Webster HDF (1970) The fine structure of the nervous system: the cells and their processes. Harper and Row, New York
Raczkowski D, Fitzpatrick D (1989) Organization of cholinergic synapses in the cat's dorsal lateral geniculate and perigeniculate nuclei. J Comp Neurol 288:676–690
Ralston HJ (1971) Evidence for presynaptic dendrites and a proposal for their mechanism of action. Nature 230:585–587
Rapisardi SC, Miles TP (1984) Synaptology of retinal terminals in the dorsal lateral geniculate nucleus of the cat. J Comp Neurol 223:515–534
Robson JA (1983) The morphology of corticofugal axons to the dorsal lateral geniculate nucleus in the cat. J Comp Neurol 216:89–103
Robson JA, Mason CA (1979) The synaptic organization of terminals traced from individual labeled retino-geniculate axons in the cat. Neuroscience 4:99–111
Sherman SM, Friedlander MJ (1988) Identification of X versus Y properties for interneurons in the A-laminae of the cat's lateral geniculate nucleus. Exp Brain Res 73:384–392
Sillito AM, Kemp JA (1983) The influence of GABAergic inhibitory processes on the receptive field structure of X and Y cells in cat dorsal lateral geniculate nucleus (dLGN). Brain Res 277:63–78
Singer W (1977) Control of thalamic transmission by corticofugal and ascending reticular pathways in the visual system. Physiol Rev 57:386–420
Singer W, Bedworth N (1974) Correlation between the effects of brain stem stimulation and saccadic eye movements on transmission in the cat lateral geniculate nucleus. Brain Res 72:185–202
Singer W, Poppel E, Creutzfeldt O (1972) Inhibitory interaction in the cat's lateral geniculate nucleus. Exp Brain Res 14:210–226
Smith Y, Paré D, Deschenes M, Parent A, Steriade M (1988) Cholinergic and non-cholinergic projections from the upper brainstem core to the visual thalamus in the cat. Exp Brain Res 69:1–15
Somogyi P, Hodgson AJ (1985) Antisera to gamma-aminobutyric acid. III. Demonstration of GABA in Golgi-impregnated neurons and in conventional electron microscopic sections of cat striate cortex. J Histochem Cytochem 33:249–257
Somogyi P, Soltesz I (1986) Immunogold demonstration of GABA in synaptic terminals of intracellularly recorded, horseradish peroxidase-filled basket cells and clutch cells in the cat's visual cortex. Neuroscience 19:1051–1065
Somogyi J, Hámori J, Silakov VL (1984) Synaptic reorganization in the lateral geniculate nucleus of the adult cat following chronic decortication. Exp Brain Res 54:485–498
Storm-Mathisen J, Leknes AK, Bore AT, Vaaland JL, Edminson P, Haug FMS, Ottersen OP (1983) First visualization of glutamate and GABA in neurones by immunocytochemistry. Nature 301:517–520
Szentágothai J, Hámori J, Tömböl T (1966) Degeneration and electron microscope analysis of the synaptic glomeruli in the lateral geniculate body. Exp Brain Res 2:283–301
Varela FJ, Singer W (1987) Neuronal dynamics in the visual corticothalamic pathway revealed through binocular rivalry. Exp Brain Res 66:10–20
Weber AJ, Kalil RE (1987) Development of corticogeniculate synapses in the cat. J Comp Neurol 264:171–192
Weber AJ, Kalil RE, Behan M (1989) Synaptic connections between corticogeniculate axons and interneurons in the dorsal lateral geniculate nucleus of the cat. J Comp Neurol 289:156–164
Wenthold R, Zempel J, Parakkal MH, Reeks KA, Altschuler RA (1986) Immunocytochemical localization of GABA in the cochlear nucleus of the guinea pig. Brain Res 380:7–18
Wilson JR, Friedlander MJ, Sherman SM (1984) Fine structural morphology of identified X- and Y- cells in the cat's lateral geniculate nucleus. Proc R Soc Lond 221:411–436