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

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.

The contribution of inferior colliculus activity to the auditory brainstem response (ABR) in mice.

In mice, the auditory brainstem response (ABR) is frequently used to assess hearing status in transgenic hearing models. The diagnostic value of the ABR depends on knowledge about the anatomical sources of its characteristic waves. Here, we studied the contribution of the inferior colliculus (IC) to the click-evoked scalp ABR in mice. We demonstrate a non-invasive correlate of the IC response that can be measured in the scalp ABR as a slow positive wave P0 with peak latency 7-8 ms when recorded with adequate band-pass filtering. Wave P0 showed close correspondence in latency, magnitude and shape with the sustained part of evoked spiking activity and local field potentials (LFP) in the central nucleus of the IC. In addition, the onset peaks of the IC response were related temporally to ABR wave V and to some extent to wave IV. This relation was further supported by depth-dependent modulation of the shape of ABR wave IV and V within the IC suggesting generation within or in close vicinity to the IC. In conclusion, the slow ABR wave P0 in the scalp ABR may represent a complementary non-invasive marker for IC activity in the mouse. Further, the latency of synchronized click-evoked activity in the IC supports the view that IC contributes to ABR wave V, and possibly also to ABR wave IV.

Cross-Modal Plasticity in Higher-Order Auditory Cortex of Congenitally Deaf Cats Does Not Limit Auditory Responsiveness to Cochlear Implants.

UNLABELLED: Congenital sensory deprivation can lead to reorganization of the deprived cortical regions by another sensory system. Such cross-modal reorganization may either compete with or complement the "original" inputs to the deprived area after sensory restoration and can thus be either adverse or beneficial for sensory restoration. In congenital deafness, a previous inactivation study documented that supranormal visual behavior was mediated by higher-order auditory fields in congenitally deaf cats (CDCs). However, both the auditory responsiveness of "deaf" higher-order fields and interactions between the reorganized and the original sensory input remain unknown. Here, we studied a higher-order auditory field responsible for the supranormal visual function in CDCs, the auditory dorsal zone (DZ). Hearing cats and visual cortical areas served as a control. Using mapping with microelectrode arrays, we demonstrate spatially scattered visual (cross-modal) responsiveness in the DZ, but show that this did not interfere substantially with robust auditory responsiveness elicited through cochlear implants. Visually responsive and auditory-responsive neurons in the deaf auditory cortex formed two distinct populations that did not show bimodal interactions. Therefore, cross-modal plasticity in the deaf higher-order auditory cortex had limited effects on auditory inputs. The moderate number of scattered cross-modally responsive neurons could be the consequence of exuberant connections formed during development that were not pruned postnatally in deaf cats. Although juvenile brain circuits are modified extensively by experience, the main driving input to the cross-modally (visually) reorganized higher-order auditory cortex remained auditory in congenital deafness. SIGNIFICANCE STATEMENT: In a common view, the "unused" auditory cortex of deaf individuals is reorganized to a compensatory sensory function during development. According to this view, cross-modal plasticity takes over the unused cortex and reassigns it to the remaining senses. Therefore, cross-modal plasticity might conflict with restoration of auditory function with cochlear implants. It is unclear whether the cross-modally reorganized auditory areas lose auditory responsiveness. We show that the presence of cross-modal plasticity in a higher-order auditory area does not reduce auditory responsiveness of that area. Visual reorganization was moderate, spatially scattered and there were no interactions between cross-modally reorganized visual and auditory inputs. These results indicate that cross-modal reorganization is less detrimental for neurosensory restoration than previously thought.

Auditory evoked bursts in mouse visual cortex during isoflurane anesthesia.

General anesthesia is not a uniform state of the brain. Ongoing activity differs between light and deep anesthesia and cortical response properties are modulated in dependence of anesthetic dosage. We investigated how anesthesia level affects cross-modal interactions in primary sensory cortex. To examine this, we continuously measured the effects of visual and auditory stimulation during increasing and decreasing isoflurane level in the mouse visual cortex and the subiculum (from baseline at 0.7 to 2.5 vol % and reverse). Auditory evoked burst activity occurred in visual cortex after a transition during increase of anesthesia level. At the same time, auditory and visual evoked bursts occurred in the subiculum, even though the subiculum was unresponsive to both stimuli previous to the transition. This altered sensory excitability was linked to the presence of burst suppression activity in cortex, and to a regular slow burst suppression rhythm (~0.2 Hz) in the subiculum. The effect disappeared during return to light anesthesia. The results show that pseudo-heteromodal sensory burst responses can appear in brain structures as an effect of an anesthesia induced state change.