Higher-order auditory areas in congenital deafness: Top-down interactions and corticocortical decoupling

Abstract

The theory of predictive coding assumes that higher-order representations influence lower-order representations by generating predictions about sensory input. In congenital deafness, one identified dysfunction is a reduced activation of deep layers in the auditory cortex. Since these layers play a central role for processing top-down influences, congenital deafness might interfere with the integration of top-down and bottom-up information flow. Studies in humans suggest more deficits in higher-order than in primary cortical areas in congenital deafness. That opens up the question how well neurons in higher-order areas can be activated by the input through the deprived auditory pathway after restoration of hearing with cochlear implants. Further it is unclear whether their interconnections to lower order areas are impaired by absence of hearing. Corticocortical anatomical fiber tracts and general auditory responsiveness in both primary and higher-order areas are generally preserved in absence of auditory experience. However, the existing data suggest a dichotomy between preservation of anatomical cortical connectivity in congenital deafness and functional deficits in corticocortical coupling. Further, cross-modal reorganization observed in congenital deafness in specific cortical areas appears to be established by functional synaptic changes and rests on anatomically preserved, genetically-predetermined and molecularly patterned circuitry connecting the sensory systems. Current data indicate a reduced corticocortical functional coupling between cortical auditory areas in congenital deafness, both in bottom-up and top-down information stream. Consequently, congenital deafness is likely to result in a deficit in predictive coding that affects learning ability after late cochlear implantation.

Congenital deafness affects deep layers in primary and secondary auditory cortex

“…On the other hand, extensive functional deficits in primary cortical field A1 of deaf animals (Hartmann, Shepherd, Heid, & Klinke, ; Raggio & Schreiner, ; Fallon et al, ; Fallon, Irvine, & Shepherd, ; Tillein et al, ; Beitel, Vollmer, Raggio, & Schreiner, ; review in Kral & Sharma, ) indicate a dichotomy between deficient neuronal function and preserved fiber tracts to A1, and point to a synaptic or cellular origin of the functional deficits (Kral et al, ). A similar dichotomy between generally preserved anatomical fiber tracts and extensive functional deficits following sensory deprivation has been noted previously in the visual system (Mower, Caplan, Christen, & Duffy, ).…”

Human Thalamic Somatosensory Nucleus (Ventral Caudal, Vc) as a Locus for Stimulation by INPUTS from Tactile, Noxious and Thermal Sensors on an Active Prosthesis

“…Therefore amputees must learn to incorporate unnatural sensations evoked by TMIS from sensor into established motor behaviors involving a part of the body which is no longer represented in the forebrain. This is a complex learning task like that of patients with hearing loss who must learn to use cochlear implants to hear [122,123]. …”

The Impact of Ecological Niche on Adaptive Flexibility of Sensory Circuitry

“…On a developmental time scale, in deaf or blind animals including humans, the intact sense takes over territory that would normally belong to the deprived or damaged sense. This produces what can seem like supernatural ability in the intact sense (Rauschecker et al, 1992; Rauschecker and Korte, 1993; Bavelier and Neville, 2002; Lomber et al, 2010; Butler et al, 2017; Glick and Sharma, 2017; Kral et al, 2017; Schormans et al, 2017). The ability of sensory cortex to reconfigure its organization and connectivity according to unforeseen circumstances would predispose it to adapt to evolutionary change (Pallas, 2007; Kral and Pallas, 2011; Pallas and Mao, 2012, for review).…”