A Transient Translaminar GABAergic Interneuron Circuit Connects Thalamocortical Recipient Layers in Neonatal Somatosensory Cortex

Marques-Smith, André; Lyngholm, Daniel; Kaufmann, Anna-Kristin; Stacey, Jacqueline A.; Hoerder‐Suabedissen, Anna; Becker, Esther B. E.; Wilson, Michael C.; Molnár, Zoltán; Butt, Simon J. B.

doi:10.1016/j.neuron.2016.01.015

Cited by 143 publications

(216 citation statements)

References 91 publications

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“…L5b Somatostatin (SST) interneurons of the earlier developing somatosensory cortex receive thalamic input and form a transient circuit to L4 during development (starting at P4) (Marques-Smith et al, 2016; Tuncdemir et al, 2016). Since our sample might include SST-neurons, translaminar excitatory circuits might couple thalamorecipient subplate and L5 SST-neurons at early ages, and both pathways converge onto L4 (Marques-Smith et al, 2016; Zhao et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

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Distinct Translaminar Glutamatergic Circuits to GABAergic Interneurons in the Neonatal Auditory Cortex

Deng

Kao

2017

Cell Reports

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Summary GABAergic activity is important in neocortical development and plasticity. Since the maturation of GABAergic interneurons is regulated by neural activity, the source of excitatory inputs to GABAergic interneurons plays a key role in development. We show by laser-scanning photostimulation that layer 4 and layer 5 GABAergic interneurons in auditory cortex in neonatal mice (< P7) receive extensive translaminar glutamatergic input via NMDAR-only synapses. Extensive translaminar AMPAR-mediated input developed during the second postnatal week while NMDAR-only presynaptic connections decreased. GABAergic interneurons showed two spatial patterns of translaminar connection: inputs originating predominantly from supragranular or from supragranular and infragranular layers including subplate which relays early thalamocortical activity. Sensory deprivation altered the development of translaminar inputs. Thus, distinct translaminar circuits to GABAergic interneurons exist throughout development and the maturation of excitatory synapses is input specific. Glutamatergic signaling from subplate and intracortical sources likely plays a role in the maturation of GABAergic interneurons.

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Section: Discussionmentioning

confidence: 99%

“…Since our sample might include SST-neurons, translaminar excitatory circuits might couple thalamorecipient subplate and L5 SST-neurons at early ages, and both pathways converge onto L4 (Marques-Smith et al, 2016; Zhao et al, 2009). Thus, ascending input from the thalamus can reach L4 via multiple pathways.…”

Section: Discussionmentioning

confidence: 99%

Distinct Translaminar Glutamatergic Circuits to GABAergic Interneurons in the Neonatal Auditory Cortex

Deng

Kao

2017

Cell Reports

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“…Interneurons have been suggested to regulate early organizational activity patterns in the cortex and hippocampus (Allene et al, 2008; Bonifazi et al, 2009; Picardo et al, 2011) and to control the expression of critical period plasticity by excitatory neurons (Takesian and Hensch, 2013). Recent work has further suggested complex developmental interactions between populations of inhibitory interneurons (Anastasiades et al, 2016; Marques-Smith et al, 2016; Tuncdemir et al, 2016). Developmental dysregulation of GABAergic cells is associated with pathophysiology underlying neurodevelopmental disorders including autism and schizophrenia, as well as epilepsy (Rossignol, 2011).…”

Section: Introductionmentioning

confidence: 99%

Developmental Dysfunction of VIP Interneurons Impairs Cortical Circuits

Batista-Brito

Vinck

Ferguson

et al. 2017

Neuron

127

110

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GABAergic interneurons play important roles in cortical circuit development. However, there are multiple populations of interneurons and their respective developmental contributions remain poorly explored. Neuregulin 1 (NRG1) and its interneuron-specific receptor ERBB4 are critical genes for interneuron maturation. Using a conditional ErbB4 deletion, we tested the role of vasoactive intestinal peptide (VIP)-expressing interneurons in the postnatal maturation of cortical circuits in vivo. ErbB4 removal from VIP interneurons during development leads to changes in their activity, along with severe dysregulation of cortical temporal organization and state-dependence. These alterations emerge during adolescence, and mature animals in which VIP interneurons lack ErbB4 exhibit reduced cortical responses to sensory stimuli and impaired sensory learning. Our data support a key role for VIP interneurons in cortical circuit development and suggest a possible contribution to pathophysiology in neurodevelopmental disorders. These findings provide a new perspective on the role of GABAergic interneuron diversity in cortical development.

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“…Future genetic and pharmacological approaches to manipulate embryonic and postnatal neurosteroids may clarify and differentiate their role in the three main classes of cortical interneurones . Similar studies are required across different cortical layers and areas (eg, visual vs somatosensory cortex) because translaminar GABAergic inhibition is subserved by different interneurone classes …”

Section: Neurosteroid Modulation Of Gabaar Function During Postnatal mentioning

confidence: 99%

Endogenous neurosteroids influence synaptic GABA_A receptors during postnatal development

Belelli

Brown

Mitchell

et al. 2018

J Neuroendocrinology

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GABA plays a key role in both embryonic and neonatal brain development. For example, during early neonatal nervous system maturation, synaptic transmission, mediated by GABA A receptors (GABA A Rs), undergoes a temporally specific form of synaptic plasticity to accommodate the changing requirements of maturing neural networks. Specifically, the duration of miniature inhibitory postsynaptic currents (mIPSCs), resulting from vesicular GABA activating synaptic GABA A Rs, is reduced, permitting neurones to appropriately influence the window for postsynaptic excitation. Conventionally, programmed expression changes to the subtype of synaptic GABA A R are primarily implicated in this plasticity. However, it is now evident that, in developing thalamic and cortical principaland inter-neurones, an endogenous neurosteroid tone (eg, allopregnanolone) enhances synaptic GABA A R function. Furthermore, a cessation of steroidogenesis, as a result of a lack of substrate, or a co-factor, appears to be primarily responsible for early neonatal changes to GABAergic synaptic transmission, followed by further refinement, which results from subsequent alterations of the GABA A R subtype. The timing of this cessation of neurosteroid influence is neurone-specific, occurring by postnatal day (P)10 in the thalamus but approximately 1 week later in the cortex. Neurosteroid levels are not static and change dynamically in a variety of physiological and pathophysiological scenarios.Given that GABA plays an important role in brain development, abnormal perturbations of neonatal GABA A R-active neurosteroids may have not only a considerable immediate, but also a longer-term impact upon neural network activity. Here, we review recent evidence indicating that changes in neurosteroidogenesis substantially influence neonatal GABAergic synaptic transmission. We discuss the physiological relevance of these findings and how the interference of neurosteroid-GABA A R interaction early in life may contribute to psychiatric conditions later in life. K E Y W O R D Scortex, GABA A receptor, neurosteroid, synaptic inhibition, thalamus

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A Transient Translaminar GABAergic Interneuron Circuit Connects Thalamocortical Recipient Layers in Neonatal Somatosensory Cortex

Cited by 143 publications

References 91 publications

Distinct Translaminar Glutamatergic Circuits to GABAergic Interneurons in the Neonatal Auditory Cortex

Distinct Translaminar Glutamatergic Circuits to GABAergic Interneurons in the Neonatal Auditory Cortex

Developmental Dysfunction of VIP Interneurons Impairs Cortical Circuits

Endogenous neurosteroids influence synaptic GABA_A receptors during postnatal development

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A Transient Translaminar GABAergic Interneuron Circuit Connects Thalamocortical Recipient Layers in Neonatal Somatosensory Cortex

Cited by 143 publications

References 91 publications

Distinct Translaminar Glutamatergic Circuits to GABAergic Interneurons in the Neonatal Auditory Cortex

Distinct Translaminar Glutamatergic Circuits to GABAergic Interneurons in the Neonatal Auditory Cortex

Developmental Dysfunction of VIP Interneurons Impairs Cortical Circuits

Endogenous neurosteroids influence synaptic GABAA receptors during postnatal development

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Product

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Endogenous neurosteroids influence synaptic GABA_A receptors during postnatal development