Intracortical Circuits in Thalamorecipient Layers of Auditory Cortex Refine after Visual Deprivation

Abstract

Sensory cortices do not work in isolation. The functional responses of neurons in primary sensory cortices can be affected by activity from other modalities. For example, short-term visual deprivations, or dark exposure (DE), leads to enhanced neuronal responses and frequency selectivity to sounds in layer 4 (L4) of primary auditory cortex (A1). Circuit changes within A1 likely underlie these changes. Prior studies revealed that DE enhanced thalamocortical transmission to L4 in A1. Since the frequency selectivity of L4 neurons is determined both by thalamocortical as well as intracortical inputs changes in intra-laminar circuits to L4 neurons might also contribute to improved sound responses. We thus investigated in mouse A1 if intra-cortical circuits to L4 cells changed after DE. Using in vitro whole-cell patch recordings in thalamocortical slices from mouse auditory cortex we show that DE can lead to refinement of inter-laminar excitatory as well as inhibitory connections from L2/3 to L4 cells, which is manifested as a weakening of these connections. The circuit refinement is present along the tonotopic axis, indicating a reduced integration along the tonotopic axis. Thus, cross-modal influences may alter the spectral and temporal processing of sensory stimuli in multiple cortical layers by refinement of thalamocortical and intracortical circuits.

Significance Statement Temporary visual deprivation leads to sharper frequency selectivity and increased sensitivity of thalamorecipient neurons in layer 4 (L4) of primary auditory cortex (A1). Although thalamocortical synapses in A1 are strengthened after visual deprivation the intracortical circuit changes underlying the functional changes in L4 are poorly understood. We here investigated the functional microcircuits targeting L4 neurons. We show that visual deprivations cause a spatial refinement of inter-laminar excitatory as well as inhibitory connections from L2/3 to L4 cells but not within L4. The circuit refinement is present along the tonotopic axis indicating a reduced integration along the tonotopic axis. Our findings show that cross-modal influences can impact the processing of sensory stimuli in L4 by adjusting both thalamocortical and intracortical circuits.