How Thalamus Connects to Spiny Stellate Cells in the Cat's Visual Cortex (original) (raw)
Related papers
Synaptic output of physiologically identified spiny stellate neurons in cat visual cortex
The Journal of Comparative Neurology, 1994
Spiny stellate neurons of area 17 of the cat's visual cortex were physiologically characterised and injected intracellularly with horseradish peroxidase. Six neurons from sublamina 4A were selected. Five had the S-type of simple receptive fields; one had a complex receptive field. Their axons formed boutons mainly in layers 3 and 4. An electron microscopic examination of 45 boutons showed that each bouton formed one asymmetric synapse on average. Spines were the most frequent synaptic target (74%); dendritic shafts formed the remainder (26%). On the basis of ultrastructural characteristics, 8% of the target dendrites were characterised as originating from smooth y-aminobutyrate-ergic (GABAergic) neurons. Thus the major output of spiny stellate neurons is to other spiny neurons, probably pyramidal neurons in layer 3 and spiny stellates in layer 4.
Map of the synapses formed with the dendrites of spiny stellate neurons of cat visual cortex
The Journal of Comparative Neurology, 1994
The synaptic input of six spiny stellate neurons in sublamina 4A of cat area 17 was assessed by electron microscopy. The neurons were physiologically characterized and filled with horseradish peroxidase in vivo. After processing the neurons were reconstructed at the light microscopic level using computer-assisted methods and analyzed quantitatively. The extensive branching of the dendritic tree about 50 km from the soma meant that the distal branches constituted five times the length of proximal dendrite. Proximal and distal portions of a single dendrite from each neuron were examined in series of ultrathin sections (1,456 sections) in the electron microscope. The majority (79%) of the 263 synapses examined were asymmetric; the remainder (21%) were symmetric. Symmetric synapses formed 35% of synapses sampled on proximal dendrites and were usually located on the shaft. They formed only 4% of synapses sampled on distal dendrites. Spines accounted for less than half of the total asymmetric synapses (45%); the remainder were on shafts. Symmetric synapses formed with four of 92 spines. Nine spines formed no synapses. Spiny stellate neurons in cat visual cortex appear to differ considerably from pyramidal neurons in having a significant asymmetric (excitatory) synaptic input to the dendritic shaft. o
Polyneuronal innervation of spiny stellate neurons in cat visual cortex
The Journal of Comparative Neurology, 1994
Our hypothesis was that spiny stellate neurons in layer 4 of cat visual cortex receive polyneuronal innervation. We characterised the synapses of four likely sources of innervation by three simple criteria: the type of synapse, the target (spine, dendritic shaft), and the area of the presynaptic bouton. The layer 6 pyramids had the smallest boutons and formed asymmetric synapses mainly with the dendritic shaft. The thalamic afferents had the largest boutons and formed asymmetric synapses mainly with spines. The spiny stellates had medium-sized boutons and formed asymmetric synapses mainly with spines. We used these to make a "template" to match against the boutons forming synapses with the spiny stellate dendrite. Of the asymmetric synapses, 45% could have come from layer 6 pyramidal neurons, 28% from spiny stellate neurons, and 6% from thalamic afferents. The remaining 21% of asymmetric synapses could not be accounted for without assuming some additional selectivity of the presynaptic axons. Additional asymmetric synapses may come from a variety of sources, including other cortical neurons and subcortical nuclei such as the claustrum. Of the symmetric synapses, 84% could have been provided by clutch cells, which form large boutons. The remainder, formed by small boutons, probably come from other smooth neurons in layer 4, e.g., neurogliaform and bitufted neurons. Our analysis supports the hypothesis that the spiny stellate receives polyneuronal innervation, perhaps from all the sources of boutons in layer 4. Although layer 4 is the major recipient of thalamic afferents, our results show that they form only a few percent of the synapses of layer 4 spiny stellate neurons. o
2009
Pyramidal cells of layer 6 in cat visual cortex are the source of the corticothalamic projection, and their recurrent collaterals provide substantially more excitatory synapses in layer 4 than does the thalamic input. They have predominantly simple receptive fields and can be driven monosynaptically by electrically stimulating thalamic relay cells. Layer 6 cells could thus provide a significant disynaptic amplification of the thalamic input to layer 4, particularly since their synapses facilitate, unlike the thalamic afferents whose synapses depress. However, purely geometric considerations of the relation of their dendritic trees to the thalamic input indicate that they should form a far smaller number of synapses with thalamic afferents than do the simple cells of layer 4. We thus analyzed quantitatively the thalamic input to identified corticothalamic cells by labeling the thalamic afferents and corticothalamic cells in vivo. We made a correlated light and electron microscopic study of 73 "contacts" between thalamic afferents and five corticothalamic cells. The electron microscope revealed that only 24 of the contacts identified at light microscope level were indeed synapses and, contrary to geometric predictions, virtually all were located on spines on the basal dendrites. Our quantitative estimates indicate that the corticothalamic cells form even fewer synapses with the thalamic afferents than predicted by geometric considerations and only 1/10 as many as do the layer 4 simple cells. These data strongly suggest it is the collective computation of cortical neurons, not the monosynaptic thalamic input, that determines the output of the corticothalamic cells.
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
Patterns of synaptic input to layer 4 of cat striate cortex
The Journal of Neuroscience, 1984
Although cells in layer 4 of cat striate cortex represent the first stage in the cortical processing of visual information, they have considerably more complicated receptive field properties than the afferents to the layer from the lateral geniculate nucleus. In considering how these properties are generated, we have focused on the intrinsic cortical circuitry, and particularly on the projection to layer 4 from layer 6. Layer 6 pyramidal cells were injected with horseradish peroxidase and examined at the light and electron microscopic level. The labeled axon terminals were found to form asymmetric synapses and to show a strong preference for contacting dendritic shafts. Serial reconstruction of dendrites postsynaptic to labeled layer 6 cell axon terminals showed that a large proportion of the postsynaptic dendrites belonged to smooth and sparsely spiny stellate cells, suggesting a selective innervation of these cell types. In contrast, the geniculate projection to layer 4 made synapses primarily with dendritic spines and, as a result, the large majority of terminals ended on spiny cells. Since smooth and sparsely spiny stellate cells are thought to mediate inhibition within the cortex, we suggest that one effect of the layer 6 to layer 4 projection could be to contribute to inhibitory features of the receptive fields of layer 4 cells.
Map of the synapses onto layer 4 basket cells of the primary visual cortex of the cat
The Journal of Comparative Neurology, 1997
The pattern of excitatory and inhibitory inputs to the inhibitory neurons is largely unknown. We have set out to quantify the major excitatory and inhibitory inputs to layer 4 basket cells from the primary visual cortex of the cat. The synapses formed with the soma, and proximal and distal dendrites, were examined at the light and electron microscopic levels in four basket cells, recorded in vivo and filled with horseradish peroxidase. The major afferents of layer 4 have been well characterised, both at the light and electron microscopic levels. The sizes of the synaptic boutons of the major excitatory inputs to layer 4 from the thalamic relay cells, spiny stellate cells, and layer 6 pyramidal neurons are statistically different. Their distributions were compared to those of the boutons forming asymmetric contacts onto the basket cells, which were assumed to be provided by the same set of excitatory afferents. The best-fit results showed that about equal numbers of synapses were provided by the layer 6 pyramids (43%) and the spiny stellates (44%), whereas the thalamic afferents contributed only 13%. A similar analysis on the symmetric synaptic input to the basket cells indicated that as much as 79% of the symmetric synapses could have originated from other layer 4 basket cells. Thalamic and spiny stellate synapses were preferentially located on the soma and proximal dendrites, regions that also had 76% of all the symmetric contacts.