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

Tamás, Gábor; Buhl, Eberhard H.; Somogyi, Péter

doi:10.1523/jneurosci.17-16-06352.1997

Cited by 194 publications

(153 citation statements)

References 43 publications

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“…Autapses are a special case of synapse found at elevated frequency in two cells, Mi1 and Dm9, and elsewhere at specific sites of various regions of the vertebrate brain (45,46). Most are thought to be inhibitory, and therefore self-limiting, maintaining the precision with which a neuron fires action potentials (46).…”

Section: Discussionmentioning

confidence: 99%

Synaptic circuits and their variations within different columns in the visual system of Drosophila

Takemura

Lǚ

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

261

379

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We reconstructed the synaptic circuits of seven columns in the second neuropil or medulla behind the fly's compound eye. These neurons embody some of the most stereotyped circuits in one of the most miniaturized of animal brains. The reconstructions allow us, for the first time to our knowledge, to study variations between circuits in the medulla's neighboring columns. This variation in the number of synapses and the types of their synaptic partners has previously been little addressed because methods that visualize multiple circuits have not resolved detailed connections, and existing connectomic studies, which can see such connections, have not so far examined multiple reconstructions of the same circuit. Here, we address the omission by comparing the circuits common to all seven columns to assess variation in their connection strengths and the resultant rates of several different and distinct types of connection error. Error rates reveal that, overall, <1% of contacts are not part of a consensus circuit, and we classify those contacts that supplement (E+) or are missing from it (E−). Autapses, in which the same cell is both presynaptic and postsynaptic at the same synapse, are occasionally seen; two cells in particular, Dm9 and Mi1, form ≥20-fold more autapses than do other neurons. These results delimit the accuracy of developmental events that establish and normally maintain synaptic circuits with such precision, and thereby address the operation of such circuits. They also establish a precedent for error rates that will be required in the new science of connectomics.neural circuits | stereotypy | biological error rates | reconstruction error rates

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Section: Discussionmentioning

confidence: 99%

Synaptic circuits and their variations within different columns in the visual system of Drosophila

Takemura

Lǚ

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

261

379

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“…8). Bitufted or bipolar interneurons in L2/3 have been described as interneurons with a polar dendritic tree, a narrow axonal projection, and adapting firing patterns (Fairén et al, 1984;Tamás et al, 1997;Reyes et al, 1998). Group local 3 interneurons matched some of these criteria of bitufted neurons.…”

Section: Comparison With Other Interneuron Classificationsmentioning

confidence: 99%

Efficient Recruitment of Layer 2/3 Interneurons by Layer 4 Input in Single Columns of Rat Somatosensory Cortex

Helmstaedter¹,

Staiger²,

Sakmann³

et al. 2008

J. Neurosci.

107

109

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Interneurons in layers 2/3 are excited by pyramidal cells within the same layer (Reyes et al., 1998; Gupta et al., 2000), but little is known about translaminar innervation of these interneurons by spiny neurons in the main cortical input layer 4 (L4). Here, we investigated (1) how efficiently L4 spiny neurons excite L2/3 interneurons via monosynaptic connections, (2) whether glutamate release from axon terminals of L4 spiny neurons depends on the identity of the postsynaptic interneuron, and (3) how L4-to-L2/3 interneuron connections compare with L4-to-L2/3 pyramidal neuron connections. We recorded from pairs of L4 spiny neurons and L2/3 interneurons in acute slices of rat barrel cortex of postnatal day 20 (P20) to P29 rats. The L4-to-L2/3 interneuron connections had an average unitary EPSP of 1.2 Ϯ 1.1 mV. We found an average of 2.3 Ϯ 0.8 contacts per connection, and the L4-to-L2/3 interneuron innervation domains were mostly column restricted. Unitary EPSP amplitudes and paired-pulse ratios in the L4-to-L2/3 interneuron connections depended on the "group" of the postsynaptic interneuron. Averaged over all L4-to-L2/3 interneuron connections, unitary EPSP amplitudes were 1.8-fold higher than in the translaminar L4-to-L2/3 pyramidal cell connections. Our results suggest that L4 spiny neurons may more efficiently recruit L2/3 interneurons than L2/3 pyramidal neurons, and that glutamate release from translaminar boutons of L4 spiny neuron axons is target cell specific.

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“…Dual recordings in the rat (Gibson et al, 1999) and cat (Tamas et al, 1998) have confirmed directly that neocortical layer IV interneurons inhibit other layer IV interneurons in their proximity. GABAergic cortical neurons can also inhibit themselves through autapses (Thomson et al, 1996;Tamas et al, 1997b). Thus, inhibitory interneurons effectively suppress each other's firing after their first spike, a mechanism that may allow for a faster recovery of the cortex from the inhibitory volley.…”

Section: Mutual Suppression Of Firing By Inhibitory Interneuronsmentioning

confidence: 99%

Diverse Types of Interneurons Generate Thalamus-Evoked Feedforward Inhibition in the Mouse Barrel Cortex

Porter¹,

Johnson²,

2001

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Sensory information, relayed through the thalamus, arrives in the neocortex as excitatory input, but rapidly induces strong disynaptic inhibition that constrains the cortical flow of excitation both spatially and temporally. This feedforward inhibition is generated by intracortical interneurons whose precise identity and properties were not known. To characterize interneurons generating feedforward inhibition, neurons in layers IV and V of mouse somatosensory ("barrel") cortex in vitro were tested in the cell-attached configuration for thalamocortically induced firing and in the whole-cell mode for synaptic responses. Identification as inhibitory or excitatory neurons was based on intrinsic firing patterns and on morphology revealed by intracellular staining. Thalamocortical stimulation evoked action potentials in ϳ60% of inhibitory interneurons but in Ͻ5% of excitatory neurons. The inhibitory interneurons that fired received fivefold larger thalamocortical inputs compared with nonfiring inhibitory or excitatory neurons. Thalamocortically evoked spikes in inhibitory interneurons followed at short latency the onset of excitatory monosynaptic responses in the same cells and slightly preceded the onset of inhibitory responses in nearby neurons, indicating their involvement in disynaptic inhibition. Both nonadapting (fast-spiking) and adapting (regular-spiking) inhibitory interneurons fired on thalamocortical stimulation, as did interneurons expressing parvalbumin, calbindin, or neither calcium-binding protein.Morphological analysis revealed that some interneurons might generate feedforward inhibition within their own layer IV barrel, whereas others may convey inhibition to upper layers, within their own or in adjacent columns. We conclude that feedforward inhibition is generated by diverse classes of interneurons, possibly serving different roles in the processing of incoming sensory information.

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

Cited by 194 publications

References 43 publications

Synaptic circuits and their variations within different columns in the visual system of Drosophila

Synaptic circuits and their variations within different columns in the visual system of Drosophila

Efficient Recruitment of Layer 2/3 Interneurons by Layer 4 Input in Single Columns of Rat Somatosensory Cortex

Diverse Types of Interneurons Generate Thalamus-Evoked Feedforward Inhibition in the Mouse Barrel Cortex

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