Laminar specific gene expression reveals differences in postnatal laminar maturation in mouse auditory, visual, and somatosensory cortex

Abstract

Proper formation of laminar structures in sensory cortexes is critical for sensory information processing. Previous studies suggested that the timing of neuronal migration and the laminar position of cortical neurons differ among sensory cortexes. How they differ during postnatal development has not been systematically investigated. Here, identifying laminas using transcription factors, we examined postnatal changes in neuronal density and distribution in presumptive primary auditory (ACx), visual (VCx), and somatosensory cortexes (SCx) in a strain of mice using immunofluorescence techniques. Development of laminar thickness and its cortical proportion differed among the sensory cortexes. Layers 2-4 defined by Cut-like homeobox 1 (Cux1)-expressing neurons were narrower, and layer 5 was wider in ACx compared to those in VCx or SCx, while Forkhead-box protein P2 (Foxp2)-defined layer 6 was wider in SCx than the other two sensory cortexes throughout postnatal development. Meanwhile, thalamocortical input layers identified by Cux1-expressing neurons formed later in ACx than in the other two cortical regions. The cell densities of ETS-related protein 81-expressing neurons increased in both lower and upper layers but at distinct timing, while those of COUP-TF-interacting protein 2 expressing neurons in the lower layers changed bidirectionally (i.e., increased or decreased) both in layer- and cortical region-specific manners. Foxp2-expressing cells in layer 6 distributed differently and declined at different timing among the sensory cortexes. Overall, we demonstrate that the maturational timing of lamina differs among the sensory cortexes and that postnatal age-dependent changes in neuronal distribution are unique to each of the sensory cortexes.

Temporal refinement of sensory‐evoked activity across layers in developing mouse barrel cortex

“…The distribution of spontaneous firing rate across layers was correlated with the distribution of cell density in cortical layers of barrel cortex, especially, highest in L4 (Meyer et al., ). Because the cortical neuronal density and the thickness of cortical layers do not change substantially from P11 to P27 (Chang, Suzuki, & Kawai, ), the comparisons of amplitudes of evoked MUA across development in this study are not strongly influenced (biased) by the change of cortical neuronal density during development. A large number of previous studies in adult barrel cortex have demonstrated that neurons are highly sensitive to velocity and acceleration of whisker stimulation with spikes rates increasing at higher stimulus velocities (Lee & Simons, ; Wilent & Contreras, ).…”

Genetic dissection of glutamatergic neuron subpopulations and developmental trajectories in the cerebral cortex

“…The forkhead/winged helix transcription factor, Foxp2 , is expressed in many CT neurons from postmitotic stage to mature cortex, and transiently expressed in a minor subset of ET neurons in the first postnatal week 64, 65 . We characterized a Foxp2-IRES-Cre KI line 66 by systemic injection of Cre dependent AAV9-DIO-GFP in 2 month old mice to reveal its brain-wide cell distribution pattern.…”

Genetic dissection of the glutamatergic neuron system in cerebral cortex

“…Foxp2 is expressed in many CT neurons from the postmitotic stage to the mature cortex 33 – 35 . In adult Foxp2-IRES-Cre mice 36 , systemic injection of Cre-dependent AAV9-DIO-GFP specifically labelled L6 PyNs; Foxp2 + cells were also found in the striatum, thalamus, hypothalamus, midbrain, cerebellum and inferior olive (Fig.…”