Cortical Oscillations and Effective Connectivity Depend on Sensory Experience

Cochlear stimulation activates the auditory cortex via thalamocortical inputs. Cortical responses are subsequently embedded into ongoing cortical processing via corticocortical connections, providing information on the context of the stimulus. Stimulus related activity is reflected in local field potentials (LFPs) in the form of evoked (phase-locked to the stimulus, reflecting the thalamic input) and induced (sensory-related, but non-phased-locked activity, representing corticocortical processing) responses. We investigated the effect of auditory experience on evoked and induced responses in the primary auditory cortex (A1) and a higher-order auditory field (posterior auditory field, PAF). We evaluated time-frequency representations (TFR) of auditory responses in adult hearing controls (HCs) and congenitally deaf cats (CDCs), the latter in absence of developmental hearing experience. Evoked and induced TFR power was calculated using wavelet analysis (Yusuf et al., 2017, Brain) and a quadratic time-frequency transform called Matching Pursuit (MP) algorithm. The later method distributes the energy of the signal over the two independent variables time and frequency, including the low frequency components without compromising resolution in both domains. Coupling strength between A1 and PAF was estimated using several computational methods.

The evoked responses appeared mainly at early latency (<100ms) while induced responses appeared more abundant at long latencies (>100ms), corresponding to their assumed role in thalamocortical vs. corticocortical processing, respectively. In HCs, electric stimulation resulted in reduced induced activity compared to acoustic stimulation, indicating the effect of the stimulation mode on the induced responses. The comparison of electrically elicited responses between HC and CDC showed no significant effect of deafness on A1 evoked responses, but a near loss of A1 and PAF induced responses in CDCs, particularly at longer latencies. Furthermore, the coupling between two recorded fields were decreased in CDCs, potentially in the top-down (PAF-A1) directed-connectivity. Congenital deafness thus affects corticocortical effective connectivity between auditory areas. Furthermore, developmental hearing experience is essential for integration of sensory input and corticocortical ongoing processing in the cortex, and thus integration of the stimuli into the context and the internal model of the environment.

Supported by Deutsche Forschungsgemeinschaft (Exc 1077).