Identified Sources and Targets of Slow Inhibition in the Neocortex

Tamás, Gábor; Lőrincz, Andrea; Simon, András; Szabadics, János

doi:10.1126/science.1082053

Cited by 325 publications

(382 citation statements)

References 33 publications

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“…Response to the signal envelope is seen up to cortical levels of both auditory and visual systems. The basic building blocks of our simple network, high-pass interneurons (41) and interneurons that use GABA B receptors on pyramidal cells (42)(43)(44)(45), are present at cortical levels, suggesting that this simple neural implementation of parallel linear and nonlinear information streams might be widespread.…”

Section: Discussionmentioning

confidence: 99%

The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope

Middleton

Longtin²,

Benda³

et al. 2006

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

100

115

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Sensory stimuli often have rich temporal and spatial structure. One class of stimuli that are common to visual and auditory systems and, as we show, the electrosensory system are signals that contain power in a narrow range of temporal (or spatial) frequencies. Characteristic of this class of signals is a slower variation in their amplitude, otherwise known as an envelope. There is evidence suggesting that, in the visual cortex, both narrowband stimuli and their envelopes are coded for in separate and parallel streams. The implementation of this parallel transmission is not well understood at the cellular level. We have identified the cellular basis for the parallel transmission of signal and envelope in the electrosensory system: a two-cell network consisting of an interneuron connected to a pyramidal cell by means of a slow synapse. This circuit could, in principle, be implemented in the auditory or visual cortex by the previously identified biophysics of cortical interneurons.parallel processing ͉ sensory systems ͉ stimulus envelopes N arrowband signals (i.e., containing power in a narrow range of frequencies) are an important class of naturalistic stimuli for visual and auditory systems and have associated with them a stimulus envelope, a slow, time-varying contrast or modulation of a sinusoidal carrier arising naturally from, for example, interference between two or more sinusoidal oscillations with similar frequencies. Amplitude-modulated signals have no power at the frequencies of the modulation; instead, they have power centered on the carrier frequency with side bands whose structure depends on the frequency content of the modulation or envelope (1). Because the actual signal contains no power at the envelope frequencies, a system that can extract information about the envelope must use nonlinear processing. An asymmetry in the single-neuron inputoutput transfer, such as rectification (1), will generate power at the envelope frequencies (2, 3). Recent studies show that visual cortical neurons in cats respond to both low spatial frequency signals and the low-frequency spatial envelopes of high-frequency signals and also suggest that information about stimuli and their envelopes take separate and mutually exclusive linear and nonlinear pathways to reach these cortical neurons (4-11). The cellular and network basis of these parallel cortical computations is not, however, understood.Apteronotus leptorhynchus generates a sinusoidal electric organ discharge (EOD) that produces an electric field around its body. Recent field studies have shown that A. leptorhynchus and related species forage in groups (12) (E. W. Tan and E. S. Fortune, personal communication). Although individual A. leptorhynchus maintain a stable EOD frequency (13), the species has a frequency range of Ϸ700-1,000 Hz. Two fish with widely spaced EOD frequencies will generate a high-frequency envelope of their EOD that is referred to as an amplitude modulation (AM) or beat. Additional fish can superimpose a slowly varying contrast on this high-...

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Section: Discussionmentioning

confidence: 99%

The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope

Middleton

Longtin²,

Benda³

et al. 2006

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

100

115

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“…A second group of local inhibitors ("local 2") had small EPSP amplitudes but showed PP depression only (0.59 Ϯ 0.21 mV; 0.7 Ϯ 0.18, respectively). The dendrites and axons of this group had similarities to neurogliaform neurons (Tamás et al, 2003) (see Discussion). The groups of lateral inhibitors ("lateral 1," "lateral 3") had relatively large EPSP amplitudes (Ͼ1 mV) and displayed PP depression.…”

Section: Target Cell Specificity Of L4-to-l2/3 Interneuron Connectionsmentioning

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.

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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“…4) (Fuentealba et al, 2008). IvyCs belong to the family of neurogliaform cells that are known to provide powerful, long-lasting inhibition to postsynaptic cells through their extremely dense axonal cloud (Tamás et al, 2003;Price et al, 2005;Szabadics et al, 2007). However, in contrast to hippocampal neurogliaform cells (Price et al, 2005), IvyCs release GABA onto the proximal dendritic region of pyramidal cells as they innervate the inner portion of stratum radiatum and stratum oriens (Fuentealba et al, 2008).…”

Section: Specific Description Of Cell Typesmentioning

confidence: 99%

“…As far as MF input properties are concerned, CA3 IvyCs were most similar to RSBCs, displaying rare but strong MF-euEPSCs on a background of lowfrequency spontaneous synaptic events. Although the properties of CA3 IvyCs will need to be studied further, it is likely that MF inputs to IvyCs contribute to the regulation of pyramidal cell dendritic excitability during behaviorally relevant network rhythms (Fuentealba et al, 2008) through slow IPSPs characteristic of neurons in the neurogliaform cell family (Tamás et al, 2003;Price et al, 2005;Szabadics et al, 2007).…”

Section: Mf Inputs To Slcs and Ivycsmentioning

confidence: 99%

Functional Specificity of Mossy Fiber Innervation of GABAergic Cells in the Hippocampus

Szabadics¹,

Soltész²

2009

J. Neurosci.

105

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One million mossy fibers in the rat provide individually sparse but functionally important synaptic connections between the dentate gyrus and hippocampus. Although the majority of mossy fiber targets are GABAergic cells, the functional organization of the feedforward GABAergic machinery modulating the interactions of granule cells and CA3 pyramidal cells are not yet understood. We used mossy fiber bouton to GABA neuron paired recordings in the CA3 to demonstrate that mossy fibers provide cell type-specific innervation to distinct GABAergic neurons with specialized intra-and extrahippocampal outputs. Our results show that mossy fibers contact the perisomatically projecting fast-spiking and regular-spiking basket cells, in addition to the dendritically projecting ivy cells, and the septum-projecting spiny stratum lucidum cells. Monosynaptic mossy fiber inputs to fast-spiking basket cells and spiny stratum lucidum cells were found to be numerous, but they were small in amplitude and displayed low transmission probabilities. In contrast, regular-spiking basket cells and ivy cells were less likely to be innervated by mossy fibers, but the amplitudes of mossy fiber EPSCs were large and the transmission probabilities were high. The dependence of the numbers and strengths of the mossy fiber inputs to CA3 GABAergic cells on the postsynaptic cell type was correlated with the frequency of the background synaptic events, so that cells with weak but numerous mossy fiber inputs received high rates of spontaneous synaptic events. Together, these results reveal the diverse components and high degree of functional specificity of the GABAergic cellular machinery underlying the dentate gyrus-CA3 interface.

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Identified Sources and Targets of Slow Inhibition in the Neocortex

Cited by 325 publications

References 33 publications

The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope

The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope

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

Functional Specificity of Mossy Fiber Innervation of GABAergic Cells in the Hippocampus

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