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

Abstract

SummaryGABAergic activity is thought to influence developing neocortical sensory circuits. Yet the late postnatal maturation of local layer (L)4 circuits suggests alternate sources of GABAergic control in nascent thalamocortical networks. We show that a population of L5b, somatostatin (SST)-positive interneuron receives early thalamic synaptic input and, using laser-scanning photostimulation, identify an early transient circuit between these cells and L4 spiny stellates (SSNs) that disappears by the end of the L4 critical period. Sensory perturbation disrupts the transition to a local GABAergic circuit, suggesting a link between translaminar and local control of SSNs. Conditional silencing of SST+ interneurons or conversely biasing the circuit toward local inhibition by overexpression of neuregulin-1 type 1 results in an absence of early L5b GABAergic input in mutants and delayed thalamic innervation of SSNs. These data identify a role for L5b SST+ interneurons in the control of SSNs in the early postnatal neocortex.

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

“…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).…”

“…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.…”

Developmental Dysfunction of VIP Interneurons Impairs Cortical Circuits

“…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).…”

Endogenous neurosteroids influence synaptic GABAA receptors during postnatal development

“…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 …”