Synaptic connection from cortical area V4 to V2 in macaque monkey (original) (raw)
Related papers
The Synaptic Connections between Cortical Areas V1 and V2 in Macaque Monkey
Journal of Neuroscience - J NEUROSCI, 2009
The primary visual cortex (V1) and V2 together form ϳ24% of the total neocortex of the macaque monkey and have each other as their major partners. The major target of the V1 projection to V2 is layer 4, where it forms clusters of boutons, which form asymmetric (excitatory) synapses mainly with dendritic spines (75%). The remainder form synapses with dendritic shafts. The synapses found on spines were often more complex, perforated postsynaptic densities than those found on dendritic shafts. The reciprocal projection from V2 to V1 targeted layers 1, 2/3, and 5 and was formed of axons of different morphologies. One axon type, originating from superficial layer pyramidal cells, had a morphology resembling those of local pyramidal cell collaterals. These axons arborized in layers 1, 2/3, and 5 of V1. Another type of axon, arborizing in layer 1, was slender (0.3 m), unbranched, unmyelinated, and uniformly covered with boutons terminaux and formed asymmetric synapses mainly with slender spines. Yet a third type of axon also confined to layer 1, was thick (Ͼ1 m), branched, heavily myelinated, and formed separate small clusters of large (ϳ1 m) en passant multisynaptic boutons that formed asymmetric synapses mainly with large flat spines. These data show the existence of a reciprocal excitatory loop between V1 and V2 that is formed by different axonal types, each with preferred layers of termination.
The Journal of Comparative Neurology, 1985
Chandelier cell axons were studied in the sensory-motor cortex of adult monkeys. The axonal fields of Golgi-impregnated chandelier cells in layer I1 in motor cortex are flattened sagittally. The vert.ical terminal portions of the axons varied both in length and in the numbers converging to form terminations of greater or lesser complexity. Golgi-impregnated plexuses were embedded in plastic and resectioned serially at 2.5-3.0 pm. A single axonal field could have as many as 400 terminal rows. All lie 3-13 pm beneath pyramidal cell somata. These terminations a m not randomly distributed but, instead, form clusters. Further resectionling the plastic sections for electron microscopy revealed that all the terminations are on the initial axon segments of pyramidal cells and all form s:ymmetric synaptic contacts. In immunocytochemical material stained for glutamic acid decarboxylase (GAD), the enzyme involved in the synthesis of GABA, GAD-positive boutons were found to form symmetric synapti'c contacts with a variety of postsynaptic elements including the axon hillocks and axon initial segments of pyramidal cells. Serial reconstructions frorn electron micrographs revealed GAD-positive terminals synapsing with the axon initial segment of pyramidal cells joined by cytoplasmic bridges and forming vertically oriented rows identical to those of chandelier cell terminals identified positively in the resectioned Golgi material. The GAD-positive terminals forming initial segment synapses were never continuous with GAD-positive terminals forming axon hillock synapses. The latter probably arise from basket cell axons. Initial segments of pyramidal cell axons in layers I1 and 111 were contacted by more GAD-positive terminals than the initial segments of pyramidal cell axons in layer V. The largest pyramidal cells in layer Ill received the most synapses. Many larger pyramidal cells, identified as callosally projecting cells by the retrograde transport of horseradish peroxidase (HRP), were shown in serial electron micrographs to possess large numbers of initial segment synapses, comparable to those seen in the immunocytochemical material. Serial reconstructions of pyramidal cell axons from axon hillock to the first myelin internode in resectioned Golgi, imrnunocytochemical and HRP material showed that the number of synapses varied from 2 to 52 for layers 11 and 111 and from 2 to 26 for layer V. The number of synapses on the axon hillocks varied from zero to 12. The variability in these terminations may be a n important factor in the shaping of the functional properties of the pyramidal cells.
The contribution of synaptic location to inhibitory gain control in pyramidal cells
Physiological Reports, 2013
The activity of pyramidal cells is controlled by two opposing forces: synaptic inhibition and synaptic excitation. Interestingly, these synaptic inputs are not distributed evenly across the dendritic trees of cortical pyramidal cells. Excitatory synapses are densely packed along only the more peripheral dendrites, but are absent from the proximal stems and the soma. In contrast, inhibitory synapses are located throughout the dendritic tree, the soma, and the axon initial segment. Thus both excitatory and inhibitory inputs exist on the peripheral dendritic tree, while the proximal segments only receive inhibition. The functional consequences of this uneven organization remain unclear. We used both optogenetics and dynamic patch clamp techniques to simulate excitatory synaptic conductances in pyramidal cells, and then assessed how their firing output is modulated by gamma-amino-butyric acid type A (GABA A) receptor activation at different regions of the somatodendritic axis. We report here that activation of GABA A receptor on the same dendritic compartment as excitatory inputs causes a rightwards shift in the function relating firing rate to excitatory conductance (the input-output function). In contrast, GABA A receptor activation proximal to the soma causes both a rightwards shift and also a reduction in the maximal firing rate. The experimental data are well reproduced in a simple, four compartmental model of a neuron with inhibition either on the same compartment, or proximal, to the excitatory drive.
The Journal of Comparative Neurology, 1989
The monosynaptic targets of different functional types of geniculocortical axons were compared in the primary visual cortex of monkeys. Single thalamocortical axons were recorded extracellularly in the white matter by using horseradish-peroxidase-filled pipettes. Their receptive fields were mapped and classified as corresponding to those of parvi-or magnocellular neurons in the lateral geniculate nucleus. The axons were then impaled and injected intraaxonally with horseradish peroxidase. Two magnocellular (MA) and two parvicellular (P A) axons were successfully recovered and reconstructed in three dimensions. The two MA axons arborised mainly in layer 4Ca, as did the two PA axons in layer 4Ct3. Few collaterals formed varicosities in layer 6. Both MA axons had two large, elongated clumps of bouton (approx. 300-500 x 600-1,200 J!m each) and a small clump. One PA axon had two clumps (each with a core appr. 200 J!m in diameter); the other had only one (appr. 150-200 J!m in diameter). The PA axon with two clumps had 1)520 boutons; the other PA axon had 1,380; one MA axon had 3,200 boutons; and those of the more extensive MA axon were not counted. The distribution of postsynaptic targets as well as the number of synapses per bouton has been established for a sample of 150 P A boutons and 173 MA boutons from serial ultrathin sections. The MA axons made on average 2.1 synapses per bouton compared to 1.79 for one PA axon and 2.6 for the other. The sample of boutons taken from the two physiological types ofaxons contacted similar proportions of dendritic spines (52-68%), shafts (33-47%») and somata (0-3%). The postsynaptic elements were further characterized by immunostaining for GABA. All postsynaptic perikarya and some of the dendrites (4.5-9.5% of all targets) were positive for the amino acid. Near the thalamic synapse GABA-negative dendritic shafts frequently contained lamellar bodies, an organelle identical in structure to spine apparatus. Dendritic shafts and spines postsynaptic to the thalamocortical boutons frequently received an adjacent synapse from GABA-immunoreactive boutons. The similarity between the magno-and parvicellular axons in their targeting of postsynaptic elements, including the GABAergic neurons) suggests that the structural basis of the physiological differences between 4Ca and 4Ct3 neurons should be sought in other aspects of the circuitry of layer 4C, such as local cortical circuits) or in the far greater horizontal extent of the thalamocortical and GABAergic axons in layer 4Ca compared to those in the t3 subdivision.
2009
The connection between the dorsal lateral geniculate nucleus (dLGN) and area 17 of the cat is a classical model for studying thalamocortical relations. We investigated the proportion of asymmetric synapses in layer 4 of area 17 of cats formed by axons of the dLGN, because this is an important morphological parameter in understanding the impact of dLGN axons on their target neurons. Although the present consensus is that this proportion is small, the exact percentage remains in doubt. Most previous work estimated that the thalamus contributes less than 10% of excitatory synapses in layer 4, but one estimate was as high as 28%. Two issues contribute to these widely different estimates, one being the tracers used, the other being the use of biased stereological approaches. We have addressed both of these issues. Thalamic axons were labeled in vivo by injections of biotinylated dextran amine into the A lamina of the dLGN of anesthetized cats. After processing, the brain was cut serially and prepared for light and electron microscopy. The density of asymmetric synapses in the neuropil and the density of synapses formed by labeled dLGN boutons were measured by using an unbiased sampling method called the physical disector. Our counts indicate that, in the fixed cat brain, there are 5.9 ؋ 10 8 ؎ 0.9 ؋ 10 8 asymmetric synapses per cubic millimeter of layer 4 in area 17, and the dLGN input provides only 6% of all asymmetric synapses in layer 4. The vast majority of synapses of layer 4 probably originate from other neurons in area 17.
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.
The synaptic bouton acts like a slat shaker
Cell Biochem Biophys, 2004
The physiological quantal responses at the neuromuscular junction and the bouton-neuron show two classes based on amplitude such that the larger class is about 10 times that of the smaller class; and, the larger class is composed of the smaller class. The ratio of the two classes changes with synaptogenesis, degeneration, nerve stimulation, and is readily altered with various challenges (ionic, tonicity, pharmacological agents). Statistical analyses demonstrate that each bouton or release site at the neruomuscular junction (NMJ) secretes a standard amount of transmitter (one quantum) with each action potential. The amount of transmitter secreted (quantal size) is frequency dependent. The quantal-vesicular-exocytotic (QVE) hypothesis posits that the packet of secreted transmitter is released from one vesicle by exocytosis. The QVE hypothesis neither explains two quantal classes and subunits nor exocytosis of only one vesicle at each site. The latter observation requires a mechanism to select one vesicle from each array. Our porocytosis hypothesis states that the quantal packet is pulsed from an array of secretory pores. A salt shaker delivers a standard pinch of salt with each shake because salt flows through all openings in the cap. The variation in the pinch of salt or transmitter decreases with an increase in array size. The docked vesicles, paravesicular matrix, and porosomes (pores) of a release site form the secretory unit. In analogy with the sacromere as the functional unit of skeletal muscle, we term the array of docked vesicles and paravesicular grid along with the array of postsynaptic receptors a synaptomere. Pulsed secretion from an array explains the substructure of the postsynaptic response (quantum). The array guarantees a constant amount of secretion with each action potential and permits a given synapse to function in different responses because different frequencies would secrete signature amounts of transmitter. Our porocytosis hypothesis readily explains a change in quantal size during learning and memory with an increase in the number of elements (docked vesicles) composing the array.
Cerebral cortex (New York, N.Y. : 1991), 2015
Excitatory connections between neocortical layer 4 (L4) and L6 are part of the corticothalamic feedback microcircuitry. Here we studied the intracortical element of this feedback loop, the L4 spiny neuron-to-L6 pyramidal cell connection. We found that the distribution of synapses onto both putative corticothalamic (CT) and corticocortical (CC) L6 pyramidal cells (PCs) depends on the presynaptic L4 neuron type but is independent of the postsynaptic L6 PC type. L4 spiny stellate cells establish synapses on distal apical tuft dendrites of L6 PCs and elicit slow unitary excitatory postsynaptic potentials (uEPSPs) in L6 somata. In contrast, the majority of L4 star pyramidal neurons target basal and proximal apical oblique dendrites of L6 PCs and show fast uEPSPs. Compartmental modeling suggests that the slow uEPSP time course is primarily the result of dendritic filtering. This suggests that the dendritic target specificity of the 2 L4 spiny neuron types is due to their different axonal ...