Functional excitatory microcircuits in neonatal cortex connect thalamus and layer 4.

The functional connectivity of the cerebral cortex is shaped by experience during development, especially during a critical period early in life. In the prenatal and neonatal cortex, transient neuronal circuits are formed by a population of subplate neurons (SPNs). However, SPNs are absent in the adult cortex. While SPNs are crucial for normal development of the cerebral cortex and of thalamocortical synapses, little is known about how they are integrated in the developing thalamocortical circuit. We therefore investigated SPNs in vitro in thalamocortical slices of A1 and medial geniculate nucleus (MGN) in mouse from postnatal day 1 (P1) to P13. We found that SPNs can fire action potentials at P1 and that their intrinsic membrane properties are mature after P5. We find that SPNs receive functional excitatory inputs from the MGN as early as P2. The MGN projections to SPNs strengthen between P2 and P13 and are capable of inducing action potentials in SPNs. Selective activation of SPNs by photostimulation produced EPSCs in layer 4 neurons, demonstrating a functional excitatory connection. Thus, SPNs are tightly integrated into the developing thalamocortical circuit and would be a reliable relay of early spontaneous and sound-evoked activity. The role of SPNs in development likely results from their strong excitatory projection to layer 4, which might function to regulate activity-dependent processes that enable mechanisms required for the functional maturation and plasticity of the developing cortex and thereby contribute to the development of normal cortical organization.