Robust but delayed thalamocortical activation of dendritic-targeting inhibitory interneurons

Tan, Zhenjun; Hu, Hang; Huang, Z. Josh; Agmon, Ariel

doi:10.1073/pnas.0710628105

Cited by 143 publications

(165 citation statements)

References 54 publications

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“…On the basis of the present findings, the higher density of FS cells in the walls appears to signify that this subregion consists of a more homogenous population of cells performing related functions such as providing feedforward inhibition (24). Conversely, the central hollow of a barrel is made up of a heterogeneous group of neurons that are likely performing different thalamocortical and intracortical whisker-activated functions (6,25). Therefore, the metabolically active subregions revealed by CO staining signify distinct functional zones (17), and these zones are based on the differential positioning of physiologically distinct neurons across a barrel column.…”

Section: Differential Distribution Of Neurons Across the Hollow And Wallmentioning

confidence: 60%

Long-term sensory deprivation selectively rearranges functional inhibitory circuits in mouse barrel cortex

Rudolph

Huntsman

2009

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

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Long-term whisker removal alters the balance of excitation and inhibition in rodent barrel cortex, yet little is known about the contributions of individual cells and synapses in this process. We studied synaptic inhibition in four major types of neurons in live tangential slices that isolate layer 4 in the posteromedial barrel subfield. Voltage-clamp recordings of layer 4 neurons reveal that fast decay of synaptic inhibition requires ␣1-containing GABAA receptors. After 7 weeks of deprivation, we found that GABA A-receptor-mediated inhibitory postsynaptic currents (IPSCs) in the inhibitory lowthreshold-spiking (LTS) cell recorded in deprived barrels exhibited faster decay kinetics and larger amplitudes in whisker-deprived barrels than those in nondeprived barrels in age-matched controls. This was not observed in other cell types. Additionally, IPSCs recorded in LTS cells from deprived barrels show a marked increase in zolpidem sensitivity. To determine if the faster IPSC decay in LTS cells from deprived barrels indicates an increase in ␣1 subunit functionality, we deprived ␣1(H101R) mutant mice with zolpidem-insensitive ␣1-containing GABA A receptors. In these mice and matched wild-type controls, IPSC decay kinetics in LTS cells were faster after whisker removal; however, the deprivation-induced sensitivity to zolpidem was reduced in ␣1(H101R) mice. These data illustrate a change of synaptic inhibition in LTS cells via an increase in ␣1-subunit-mediated function. Because ␣1 subunits are commonly associated with circuitspecific plasticity in sensory cortex, this switch in LTS cell synaptic inhibition may signal necessary circuit changes required for plastic adjustments in sensory-deprived cortex.interneurons ͉ networks ͉ plasticity S ynaptic inhibition is involved in sensory processing at the very first stage of cortical integration in layer 4 of the rodent primary somatosensory (barrel) cortex (1). Both feedforward and feedback inhibition from local circuit inhibitory neurons regulates the integration of thalamic and intracortical inputs (2, 3). Inhibitory neurons are distinguished from each other by action potential firing properties, morphology, and biochemical expression (4, 5). Cortical inhibitory neurons are largely separated into two functional circuits that are thought to carry out two intertwined yet separate functions in sensory processing (6). Fast-spiking (FS) cells are either basket cells or chandelier cells and express parvalbumin (4). They are readily activated by thalamic afferents and are the primary mediator of thalamocortical feedforward inhibition, and recurrent synaptic inhibition onto FS cells is very fast (6, 7). Low-threshold-spiking (LTS) cells express varying combinations of somatostatin, vasoactive intestinal peptide, and cholecystokinin (4), are weakly activated by thalamic afferents, and contribute to intracortical inhibitory transmission, and recurrent synaptic inhibition onto LTS cells decays slowly (7,8).In cortex and other regions, an emerging feature in brain networks is the ''G...

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Section: Differential Distribution Of Neurons Across the Hollow And Wallmentioning

confidence: 60%

Long-term sensory deprivation selectively rearranges functional inhibitory circuits in mouse barrel cortex

Rudolph

Huntsman

2009

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

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“…Such a scenario was recently recognized in head-restrained mice whereby fast-spiking, PV-containing, GABA interneurons markedly reduced their firing rate during active whisking, whereas that of nonfast spiking cells, which encompass VIP interneurons, greatly increased, making these interneurons the dominant source of cortical inhibition during whisking (Gentet et al, 2010). Another contributing factor could be that PV neurons receive depressing glutamatergic input from the thalamus (Tan et al, 2008). Hence, our findings, together with recent studies on different subcortical or corticocortical afferent pathways and ensuing hypermic responses (Kocharyan et al, 2008;Enager et al, 2009), emphasize that the activated cortical circuitry is both afferent and stimulus specific, as distinct subsets of cortical neurons were recruited depending on the input.…”

Section: Identity Of the Cortical Neuronal Circuitry Recruited By Whimentioning

confidence: 98%

Pyramidal Neurons Are "Neurogenic Hubs" in the Neurovascular Coupling Response to Whisker Stimulation

Lecrux

Toussay

Kocharyan

et al. 2011

Journal of Neuroscience

151

165

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The whisker-to-barrel cortex is widely used to study neurovascular coupling, but the cellular basis that underlies the perfusion changes is still largely unknown. Here, we identified neurons recruited by whisker stimulation in the rat somatosensory cortex using double immunohistochemistry for c-Fos and markers of glutamatergic and GABAergic neurons, and investigated in vivo their contribution along with that of astrocytes in the evoked perfusion response. Whisker stimulation elicited cerebral blood flow (CBF) increases concomitantly with c-Fos upregulation in pyramidal cells that coexpressed cyclooxygenase-2 (COX-2) and GABA interneurons that coexpressed vasoactive intestinal polypeptide and/or choline acetyltransferase, but not somatostatin or parvalbumin. The evoked CBF response was decreased by blockade of NMDA (MK-801, Ϫ37%), group I metabotropic glutamate (MPEPϩLY367385, Ϫ40%), and GABA-A (picrotoxin, Ϫ31%) receptors, but not by GABA-B, VIP, or muscarinic receptor antagonism. Picrotoxin decreased stimulus-induced somatosensory evoked potentials and CBF responses. Combined blockade of GABA-A and NMDA receptors yielded an additive decreasing effect (Ϫ61%) of the evoked CBF compared with each antagonist alone, demonstrating cooperation of both excitatory and inhibitory systems in the hyperemic response. Blockade of prostanoid synthesis by inhibiting COX-2 (indomethacin, NS-398), expressed by ϳ40% of pyramidal cells but not by astrocytes, impaired the CBF response (Ϫ50%). The hyperemic response was also reduced (Ϫ40%) after inhibition of astroglial oxidative metabolism or epoxyeicosatrienoic acids synthesis. These results demonstrate that changes in pyramidal cell activity, sculpted by specific types of inhibitory GABA interneurons, drive the CBF response to whisker stimulation and, further, that metabolically active astrocytes are also required.

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“…The latter interneurons will be the main source of inhibition in the late phase of TC excitation because their synaptic efficacy is maximal at this point in time. Such change in the recruitment of inhibition will also occur at stimulation frequencies of 10-20 Hz, which are behaviourally relevant whisking frequencies in rodents [168]. It should be noted, however, that in layer 4 of the barrel cortex SOM + -FS interneuron connections have been shown to exert a disinhibitory effect on the excitatory neuronal network.…”

Section: Layermentioning

confidence: 98%

“…This may contribute to an enhancement of disinhibition of a network silenced by FS interneurons. However, this action may be counteracted by SOM + interneurons in layer 5 (see below; [168]). …”

Section: Layermentioning

confidence: 99%

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Synaptic Microcircuits in the Barrel Cortex

Radnikow

Feldmeyer

2015

Sensorimotor Integration in the Whisker System

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An elementary feature of sensory cortices is thought to be their organisation into functional signal-processing units called 'cortical columns'. These elementary units process sensory information arriving from peripheral receptors; they are vertically oriented throughout all cortical layers and contain several thousands of excitatory and inhibitory synaptic connections. To understand how sensory signals are transformed into electrical activity in the neocortex it is necessary to elucidate the spatial-temporal dynamics of cortical signal processing and the underlying neurons and synaptic 'microcircuits'.In the somatosensory barrel cortex there appears to be a structural correlate for the 'functional' cortical column. Therefore, it has become an attractive model system to study the synaptic microcircuitry in the neocortex. Although many synaptic connections in whisker-related cortical 'columns' have been characterised over the past years our knowledge is far from complete, in particular with respect to inhibitory connections. In this chapter we will summarise recent data on different excitatory and inhibitory synaptic connections in a whisker-related 'column' of the somatosensory cortex and try to outline their function in the neuronal network. This requires an appreciation of the diverse types of excitatory and inhibitory neurons and their function within cortical columns and beyond. When necessary, we will also discuss the synaptic input from and to subcortical structures, in particular the thalamus. However, we will not provide a detailed description of the functional mechanisms of these connections; this is beyond the scope of this chapter.

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Robust but delayed thalamocortical activation of dendritic-targeting inhibitory interneurons

Cited by 143 publications

References 54 publications

Long-term sensory deprivation selectively rearranges functional inhibitory circuits in mouse barrel cortex

Long-term sensory deprivation selectively rearranges functional inhibitory circuits in mouse barrel cortex

Pyramidal Neurons Are "Neurogenic Hubs" in the Neurovascular Coupling Response to Whisker Stimulation

Synaptic Microcircuits in the Barrel Cortex

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