Cross-modal Plasticity in Deafness
 
 

William Molyneux asked 1688 John Locke whether a congenitally blind person who learned to distinguish between and name a sphere and a cube by touch alone, would be able to recognize these visually, if regaining the sight late in life. This famous „Molyneux Question“ has been one focus of research of our group in the recent years. It is known that the remaining sensory systems compensate the loss of one modality. But how do the remaining sensory systems affect the development of the deprived parts of the brain, and how does this affect outcome of cochlear implantation?


We were intrigued to find that the primary auditory cortex does not respond to moving and patterned visual stimuli in congenitally deaf cats (Kral et al., 2003), contrary to previous beliefs. This was despite the fact that the primary auditory cortex demonstrated numerous deficits in processing of auditory inputs (via cochlear implants) and despite visual compensations of deafness in human subjects.


 

In this context we developed the concept of corticocortical „decoupling“. In collaboration with Steve Lomber and Alex Meredith in behaving animals we could demonstrate that the capacity of different areas for cross-modal reorganization is different: some auditory areas take over some visual functions, other auditory areas are not involved in the same functions (Lomber et al., 2010). Higher-order field PAF was responsible for supranormal visual localization abilities in deaf cats, higher-order field DZ for supranormal movement detection ability. Primary fields A1 and AAF, directly neighboring fields DZ and PAF, were not involved in visual cross-modal reorganizations. This finding further supports our previous data showing that field A1 is found functionally decoupled from other auditory areas in deafness (review in Kral et al., 2006; Kral & Eggermont, 2007). Interestingly, in cross-modal reorganization even layer-specific effects have been observed (Lomber et al., 2011). Anatomical tracing experiments demonstrate a small visual reorganization of the involved area DZ, but show also a preserved connection to the auditory system (Barone et al., 2013).


Based on the above anatomical data, we performed simultaneous recordings in area DZ and neighboring visual areas that send ectopic projections to DZ (Land et al., 2016). In the field DZ of deaf animals there was increased responsiveness to visual stimulation, corresponding to the behavioral cross-modal reorganization. However, despite of this, there was no reduction of the responsiveness to cochlear implant stimulation in the same auditory field. This clearly demonstrates that cross-modal reorganization does not eliminate the auditory nature of the reorganized fields and that therapy of hearing loss is not directly limited by cross-modal reorganization. However, none of the visually responsive units was auditorily-responsive. Consequently, cross-modal reorganization is in principle limiting auditory properties, only the overall extend of the effect is modest. The data suggest that it is the exuberant connections that transiently appear in normal hearing animals and become eliminated (pruned) later in life that constitute the substrate of cross-modal reorganization in congenitally deaf. These connection are likely preserved and cause visual responsiveness and supranormal visual behavior in congenital deafness. 


We have additionally investigated the consequences of congenital deafness for auditory responsiveness in higher-order visual areas that normally show some auditory responsiveness that provides the substrate for auditory influences on visual perception. While this responsiveness has been reduced, it was not completely eliminated in congenitally deaf cats (Land et al.,2018). This demonstrates that nature may dominate over nurture: in case of many years of complete deafness, the auditory projections to an area dominated by visual inputs, and continuously activated by these, were not eliminated. This is a very surprising finding that open new research questions for our team.






Result of a tracing experiment in a normal hearing control (top) and a congenitally deaf cat (bottom). Stained cells are shown in yellow and blue. From Barone et al. (2013).

Investigation of neuronal response to visual and cochlear implant stimulation in a secondary auditory areas (field DZ) and a nearby visual area (MLS) in hearing (green) and congenitally deaf (red) animals. Left: SMI-32 staining with DiI stain (red) in the field DZ left by the multielectrode recording array (orientation of penetration shown by the green dashed lines). Rigt: Position of all penetrations in the nine animals investigated. Figure from Land et al. (2016).

Supranormal visual function and ectopic connections

Result of mapping of a higher-order visual area (AMLS/PMLS) in hearing controls (top) and congenitally deaf cats (bottom) documents reduced, but partially preserved, auditory responsiveness (Land et al., 2018). Circle diameter correspond to number of recording positions with auditory responses (inset right), circle position the approximate location of the penetration along the rostro-caudal dimension.

Mapping of a secondary auditory areas (dorsal auditory cortex, DZ) and a higher-order visual area (AMLS/PMLS) in hearing and congenitally deaf cats using linear multielectrode arrays. Each penetration included 16 recording contacts. Left: schematic illustration of the anatomical positions. Middle: reconstruction of a DiI-stained penetration, overlay of fluorescence image and Nissl-staining in DZ. Circles document position of the recording contacts. Right: Same reconstruction in AMLS. Figure from Land et al. (2018).