Indirect pathway between the primary auditory and visual cortices through layer V pyramidal neurons in V2L in mouse and the effects of bilateral enucleation

Visual cortical areas are activated by auditory stimuli in blind mice. Direct heteromodal cortical connections have been shown between the primary auditory cortex (A1) and primary visual cortex (V1), and between A1 and secondary visual cortex (V2). Auditory afferents to V2 terminate in close proximity to neurons that project to V1, and potentially constitute an effective indirect pathway between A1 and V1. In this study, we injected a retrograde adenoviral vector that expresses enhanced green fluorescent protein under a synapsin promotor in V1 and biotinylated dextran amine as an anterograde tracer in A1 to determine: (i) whether A1 axon terminals establish synaptic contacts onto the lateral part of V2 (V2L) neurons that project to V1; and (ii) if this indirect cortical pathway is altered by a neonatal enucleation in mice. Complete dendritic arbors of layer V pyramidal neurons were reconstructed in 3D, and putative contacts between pre-synaptic auditory inputs and postsynaptic visual neurons were analysed using a laser-scanning confocal microscope. Putative synaptic contacts were classified as high-confidence and low-confidence contacts, and charted onto dendritic trees. As all reconstructed layer V pyramidal neurons received auditory inputs by these criteria, we conclude that V2L acts as an important relay between A1 and V1. Auditory inputs are preferentially located onto lower branch order dendrites in enucleated mice. Also, V2L neurons are subject to morphological reorganizations in both apical and basal dendrites after the loss of vision. The A1-V2L-V1 pathway could be involved in multisensory processing and contribute to the auditory activation of the occipital cortex in the blind rodent.