The axo-axonic interneuron in the cerebral cortex of the rat, cat and monkey

Somogyi, Péter; Freund, Tamás F.; Cowey, Alan

doi:10.1016/0306-4522(82)90086-0

Cited by 364 publications

(240 citation statements)

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“…Second, the degree of autaptic innervation greatly varies between different types of cell, although there is a substantial overlap between the dendritic and axonal arborizations in all cell types tested. Although within the dendritic tree the density of GABAergic boutons originating from a single cell is higher than that of pyramidal and spiny stellate cells, this alone does not explain the high incidence of autapses, because axo-axonic cells do not form autapses (Somogyi et al, 1982;Freund et al, 1983), and DBCs only exceptionally seem to establish self-innervation despite the high density of their axons. Third, the subcellular domain-specific innervation of a cell seems to be preserved in the autaptic innervation; "forbidden" cell regions are not targeted by autapses, even when membrane apposition provides an opportunity.…”

Section: Self-innervation Is Cell Type-and Domain-specificmentioning

confidence: 95%

Massive Autaptic Self-Innervation of GABAergic Neurons in Cat Visual Cortex

1997

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Autapses are transmitter release sites made by the axon of a neuron on its own dendrites. We determined the numbers and precise subcellular position of autapses on different spiny and smooth dendritic cell types using intracellular biocytin filling in slices of adult neocortex.Potential self-innervation was light microscopically assessed on 10 pyramidal cells, 7 spiny stellate cells, and 41 smooth dendritic neurons from cortical layers II-V. Putative autapses occurred on each smooth dendritic neuron and on seven pyramids, but not on spiny stellate cells. However, electron microscopic examination of all light microscopically predicted sites on pyramids (n ϭ 28) showed only one case of self-innervation with two autapses on dendritic spines. Interneurons were classified by postsynaptic target distribution (Tamá s et al., 1997) and all putative autapses of seven basket, three dendrite-targeting, and three double bouquet cells were scrutinized. All basket and dendrite-targeting cells established self-innervation, the number of autapses being 12 Ϯ 7 and 22 Ϯ 12 (mean Ϯ SD), respectively; only one of the double bouquet cells formed autapses (n ϭ 3). Basket cell autapses (n ϭ 74) were closer to the soma (12.2 Ϯ 22.3 m) than autapses established by dendrite-targeting cells (51.8 Ϯ 49.9 m; n ϭ 66).The degree of self-innervation is cell type-specific. Unlike on spiny cells, autapses are abundant on GABAergic basket and dendrite-targeting interneurons, with subcellular location similar to that of synapses formed by the parent cell on other neurons. The extensive self-innervation may modulate integrative properties and/or the firing rhythm of the neuron in a manner temporally correlated with its own activity.

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Section: Self-innervation Is Cell Type-and Domain-specificmentioning

confidence: 95%

Massive Autaptic Self-Innervation of GABAergic Neurons in Cat Visual Cortex

1997

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“…Chandelier cells make symmetric synapses with the axonal initial segment of pyramidal cells (Somogyi et al, 1982). We assume that the chandelier cells and their axons are located primarily in layers 2/3 (Fairen and Valverde, 1980;Somogyi et al, 1982), and we ignore synapses formed in the remaining layers.…”

Section: Synapses Made By Chandelier Cells ( J ϭ J Axo2/3 )mentioning

confidence: 99%

“…We assume that the chandelier cells and their axons are located primarily in layers 2/3 (Fairen and Valverde, 1980;Somogyi et al, 1982), and we ignore synapses formed in the remaining layers. The synapses formed by the chandelier cells (S j u axo2/3 ) distribute on the axon initial segments of the pyramidal cells in layer 2/3 (i p2/3 ).…”

Section: Synapses Made By Chandelier Cells ( J ϭ J Axo2/3 )mentioning

confidence: 99%

“…Anatomical studies indicate that the total number of synapses formed by the chandelier cells on the axon initial segment is between 20 and 43 (Somogyi et al, 1982;Farinas and DeFelipe, 1991 (Beaulieu and Colonnier, 1983;Gabbott and Somogyi, 1986), and S j u axo2/3 ϭ 3300 ϫ n j axo2/3 because a chandelier cell forms ϳ3300 synapses in layer 2/3 (Somogyi et al, 1982;Freund et al, 1983). …”

Section: Synapses Made By Chandelier Cells ( J ϭ J Axo2/3 )mentioning

confidence: 99%

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A Quantitative Map of the Circuit of Cat Primary Visual Cortex

Binzegger¹,

Douglas²,

Martin³

2004

J. Neurosci.

800

996

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We developed a quantitative description of the circuits formed in cat area 17 by estimating the "weight" of the projections between different neuronal types. To achieve this, we made three-dimensional reconstructions of 39 single neurons and thalamic afferents labeled with horseradish peroxidase during intracellular recordings in vivo. These neurons served as representatives of the different types and provided the morphometrical data about the laminar distribution of the dendritic trees and synaptic boutons and the number of synapses formed by a given type of neuron. Extensive searches of the literature provided the estimates of numbers of the different neuronal types and their distribution across the cortical layers. Applying the simplification that synapses between different cell types are made in proportion to the boutons and dendrites that those cell types contribute to the neuropil in a given layer, we were able to estimate the probable source and number of synapses made between neurons in the six layers. The predicted synaptic maps were quantitatively close to the estimates derived from the experimentalelectronmicroscopicstudiesforthecaseofthemainsourcesofexcitatoryandinhibitoryinputtothespinystellatecells,whichform a major target of layer 4 afferents. The map of the whole cortical circuit shows that there are very few "strong" but many "weak" excitatory projections, each of which may involve only a few percentage of the total complement of excitatory synapses of a single neuron.

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“…Their synaptic boutons contact mainly dendritic shafts and spines on the side branches of apical dendrites as well as on basal dendrites of pyramidal neurons (Somogyi and Cowey 1981;Somogyi et al 1982;de Lima and Morrison 1989;DeFelipe et al 1989bDeFelipe et al , 1990. Their density is so high that double bouquet neurons are probably an important source of GABAergic synapses on pyramidal neurons in layer III.…”

Section: -D Endritic I Nhibitory and D Isinhibitory S Yn-apses (D Oubmentioning

confidence: 99%

GABAergic Interneurons Implications for Understanding Schizophrenia and Bipolar Disorder

Beneš

Berretta

2001

Neuropsychopharmacology

996

643

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Neurons that express the compound, ␥ -aminobutyric acid (GABA), are broadly present throughout the central nervous system, although telencephalic structures, such as the cerebral cortex, show the most abundant quantities of this neurotransmitter (Jones 1987). In the discussion that follows, the anatomy and physiology of various types of GABAergic interneurons in the cortex and hippocampus will be discussed and related to recent postmortem studies implicating this transmitter system in the pathophysiology of schizophrenia and bi- 25 , NO . 1 polar disorder and their treatment with neuroleptic drugs (for more comprehensive reviews on cortical and hippocampal neurons see: Hof et al. 1993;Freund and Buzsaki 1996;Somogyi et al. 1998). NEUROBIOLOGY OF GABAERGIC INTERNEURONSBased on Golgi-impregnation studies, Ramon y Cajal provided the first descriptions of several different morphological subtypes of interneurons in the cerebral cortex and hippocampus (Ramon y Cajal 1893, 1911. In more recent years, it has been shown that, with some overlap, different morphological subtypes also have distinct distributions, connectivity, neurochemistry, and electrophysiological properties (for reviews see Hof et al. 1993;Freund and Buzsaki 1996). It is interesting to note that every segment of a pyramidal neuron, such as the soma, dendritic branches and spines, and the initial axonal segment, receives dense GABAergic synaptic innervation (O'Kusky and Colonnier 1982;Hendry et al. 1983;Houser et al. 1983; Beaulieu et al. 1992; for reviews see Jones 1993;Freund and Buzsaki 1996). Even more interestingly, each of these segments appears to be innervated by distinct GABAergic neuronal subtypes (see below).These differences strongly suggest that each of these subtypes plays a fundamentally different role in physiological and pathological mechanisms. In the discussion that follows, cortical interneurons will be described first, since our most basic understanding of GABAergic cells is derived from these populations. In more recent years, however, similar characterizations of interneurons in hippocampus have emerged. Although these cells show some striking similarities to their cortical counterparts, there are also some unique features that distinguish them. For this reason, interneurons in the hippocampus are discussed separately. Cortex Neuroanatomical Studies of Cortical Interneurons.Various types of GABAergic neurons can be categorized according to the type of synaptic profiles they are associated with, as this has direct implications for understanding the physiological role of these cells in cortical circuits. These categories are discussed below.A XO -S OMATIC I NHIBITORY S YNAPSES (B ASKET C ELLS ). The most commonly encountered interneurons ( Figure 1A) are multipolar in shape, i.e., they may have three or more primary dendritic branches emanating from their cell bodies, some having somata that are as large as those of pyramidal neurons (Jones and Hendry 1984). Using immunocytochemistry to localize the enzyme ). These cells also ...

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The axo-axonic interneuron in the cerebral cortex of the rat, cat and monkey

Cited by 364 publications

References 42 publications

Massive Autaptic Self-Innervation of GABAergic Neurons in Cat Visual Cortex

Massive Autaptic Self-Innervation of GABAergic Neurons in Cat Visual Cortex

A Quantitative Map of the Circuit of Cat Primary Visual Cortex

GABAergic Interneurons Implications for Understanding Schizophrenia and Bipolar Disorder

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