Loss of a sensory modality can lead to functional enhancement of the remaining senses. For example, short-term visual deprivations, or dark exposure (DE), can enhance neuronal responses in the auditory cortex to sounds. These enhancements encompass increased spiking rates and frequency selectivity as well as increased spiking reliability. Although we previously demonstrated enhanced thalamocortical transmission after DE, increased synaptic strength cannot account for increased frequency selectivity or reliability. We thus investigated whether other changes in the underlying circuitry contributed to improved neuronal responses. We show that DE can lead to refinement of intra- and inter-laminar connections in the mouse auditory cortex. Moreover, we use a computational model to show that the combination of increased transmission and circuit refinement can lead to increased firing reliability. Thus cross-modal influences can alter the spectral and temporal processing of sensory stimuli by refinement of thalamocortical and intracortical circuits.