Auditory cortical plasticity under operation: Reorganization of auditory cortex induced by electric cochlear stimulation reveals adaptation to altered sensory input statistics

Theoretical Biology, Institute for Neuroinformatics, Ruhr-University Bochum, ND 04, D-44780 Bochum, Germany
Speech Communication (Impact Factor: 1.26). 08/2003; 41(1):201-219. DOI: 10.1016/S0167-6393(02)00104-8
Source: DBLP


We introduce a framework based on plastic-adaptational processes for an interpretation of electrical cochlear implant (CI) stimulation. Cochlear prostheses are used to restore sound perception in adults and children with profound deafness. After providing a review of cortical plasticity, we summarize our findings using optical imaging of intrinsic signals to map cat auditory cortex (AI) activated by CI stimulation. In adult AI of neonatally deafened animals, the acoustic deprivation caused a severe distortion of cochleotopic maps. A three-month period of CI-stimulation using the continuous interleaved sampling strategy did not re-install the status typically found in normal adults, but resulted in the emergence of a new topographical organization characterized by large, joint representations of all stimulated electrode sites. We suggest that the effectiveness of CI-stimulation relies primarily on a re-learning of input pattern arising from “artificial” sensory inputs via electrical stimulation, thereby supporting the importance of learning and training for the interpretation and understanding of the effects of CI stimulation. We suggest that the ability for gaining/re-gaining speech understanding mediated by CI-stimulation is accomplished by new strategies of cortical processing due to enhanced cooperativity among large populations of neurons that serve higher processing stages to interpret new patterns arriving from the periphery. These strategies are thought to emerge from adaptational capacities in response to the constraints imposed by the properties of the new input statistics that in turn result from the stimulation strategy employed.

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    • "Prolonged periods of profound deafness, with or without chronic ES, resulted in a three-fold increase in the area of cortex that responded to a stimulus 2 dB above the minimum cortical threshold. This increase in cortical spread is in agreement with other studies (Dinse et al., 1997, 2003; Klinke et al., 1999; Kral and Tillein, 2006), and has been interpreted as a degradation of the cochleotopic organization of the cortex (Raggio and Schreiner, 1999). These results are in contrast to the normal spread of activation in the central nucleus of the inferior colliculus after a long-term SNHL, with or without chronic multichannel stimulation (Leake et al., 2000; Snyder et al., 1990). "
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    ABSTRACT: Electrical stimulation of spiral ganglion neurons in a deafened cochlea, via a cochlear implant, provides a means of investigating the effects of the removal and subsequent restoration of afferent input on the functional organization of the primary auditory cortex (AI). We neonatally deafened 17 cats before the onset of hearing, thereby abolishing virtually all afferent input from the auditory periphery. In seven animals the auditory pathway was chronically reactivated with environmentally derived electrical stimuli presented via a multichannel intracochlear electrode array implanted at 8 weeks of age. Electrical stimulation was provided by a clinical cochlear implant that was used continuously for periods of up to 7 months. In 10 long-term deafened cats and three age-matched normal-hearing controls, an intracochlear electrode array was implanted immediately prior to cortical recording. We recorded from a total of 812 single unit and multiunit clusters in AI of all cats as adults using a combination of single tungsten and multichannel silicon electrode arrays. The absence of afferent activity in the long-term deafened animals had little effect on the basic response properties of AI neurons but resulted in complete loss of the normal cochleotopic organization of AI. This effect was almost completely reversed by chronic reactivation of the auditory pathway via the cochlear implant. We hypothesize that maintenance or reestablishment of a cochleotopically organized AI by activation of a restricted sector of the cochlea, as demonstrated in the present study, contributes to the remarkable clinical performance observed among human patients implanted at a young age.
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