Competition and convergence between auditory and cross-modal visual inputs to primary auditory cortical areas

Abstract

Sensory neocortex is capable of considerable plasticity after sensory deprivation or damage to input pathways, especially early in development. Although plasticity can often be restorative, sometimes novel, ectopic inputs invade the affected cortical area. Invading inputs from other sensory modalities may compromise the original function or even take over, imposing a new function and preventing recovery. Using ferrets whose retinal axons were rerouted into auditory thalamus at birth, we were able to examine the effect of varying the degree of ectopic, cross-modal input on reorganization of developing auditory cortex. In particular, we assayed whether the invading visual inputs and the existing auditory inputs competed for or shared postsynaptic targets and whether the convergence of input modalities would induce multisensory processing. We demonstrate that although the cross-modal inputs create new visual neurons in auditory cortex, some auditory processing remains. The degree of damage to auditory input to the medial geniculate nucleus was directly related to the proportion of visual neurons in auditory cortex, suggesting that the visual and residual auditory inputs compete for cortical territory. Visual neurons were not segregated from auditory neurons but shared target space even on individual target cells, substantially increasing the proportion of multisensory neurons. Thus spatial convergence of visual and auditory input modalities may be sufficient to expand multisensory representations. Together these findings argue that early, patterned visual activity does not drive segregation of visual and auditory afferents and suggest that auditory function might be compromised by converging visual inputs. These results indicate possible ways in which multisensory cortical areas may form during development and evolution. They also suggest that rehabilitative strategies designed to promote recovery of function after sensory deprivation or damage need to take into account that sensory cortex may become substantially more multisensory after alteration of its input during development.

Compromise of Auditory Cortical Tuning and Topography after Cross-Modal Invasion by Visual Inputs

“…Surgical procedures to induce cross-modal plasticity were similar to those described previously (Pallas et al, 1999; Mao et al, 2011). All invasive procedures were performed under sterile conditions.…”

“…Animals were prepared for electrophysiology experiments as described previously (Mao et al, 2011). The ear canals of each ferret were examined before surgery with an otoscope and cleaned if necessary.…”

“…For calculating the spatial distribution of frequency-tuned neurons, the area of each AC was normalized to a standard circle with a radius of 1 (Fig. 1)(see Mao et al, 2011). The locations of recorded units were reconstructed on this normalized AC.…”

“…Animal models employing deafness have yielded crucial information (e.g., Kral, 2007; Lomber et al, 2010) but do not allow study of competitive interactions between auditory and cross-modal visual inputs to auditory cortex. Our approach of partial midbrain damage reroutes retinal axons to auditory thalamus, placing visual and auditory inputs in a controlled state of competition (Sur et al, 1988; Pallas et al, 1999; Mao et al, 2011), while still allowing sensory activation of both modalities, thus enabling study of the effects of different degrees of cross-modal plasticity on residual auditory function.…”

Acute lesions of primary visual cortical areas in adult cats inactivate responses of neurons in higher visual cortices

“…All surgical procedures were similar to those described previously (Hua et al, 2009;Mao et al, 2011;Zhou et al, 2011). Briefly, cats were adequately anesthetized prior to preparation for single-or multi-unit recording, and the skull over the marginal and posterolateral gyri were maximally exposed and removed with a scalpel.…”