Cortical Plasticity after Cochlear Implantation

Hindawi Publishing Corporation Neural Plasticity Volume 2013, Article ID 318521, 11 pages http://dx.doi.org/10.1155/2013/318521 Research Article Cortical Plasticity after Cochlear Implantation B. Petersen,1,2 A. Gjedde,1,3 M. Wallentin,1,4 and P. Vuust1,2 1 Center for Functionally Integrative Neuroscience, Aarhus University Hospital, Nørrebrogade 44, Building 10G 6th, 8000 Aarhus C, Denmark 2 Royal Academy of Music, Skovgaardsgade 2a, 8000 Aarhus C, Denmark 3 Department of Neuroscience and Pharmacology, University of Copenhagen, Blegdamsvej 3, 2200 København N, Denmark 4 Center for Semiotics, Aarhus University, Building 1485, Office 620, Jens Chr. Skous Vej, 8000 Aarhus C, Denmark Correspondence should be addressed to B. Petersen; Received 7 July 2013; Accepted 4 October 2013 Academic Editor: Anthony J Hannan Copyright © 2013 B. Petersen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The most dramatic progress in the restoration of hearing takes place in the first months after cochlear implantation. To map the brain activity underlying this process, we used positron emission tomography at three time points: within 14 days, three months, and six months after switch-on. Fifteen recently implanted adult implant recipients listened to running speech or speech-like noise in four sequential PET sessions at each milestone. CI listeners with postlingual hearing loss showed differential activation of left superior temporal gyrus during speech and speech-like stimuli, unlike CI listeners with prelingual hearing loss. Furthermore, Broca’s area was activated as an effect of time, but only in CI listeners with postlingual hearing loss. The study demonstrates that adaptation to the cochlear implant is highly related to the history of hearing loss. Speech processing in patients whose hearing loss occurred after the acquisition of language involves brain areas associated with speech comprehension, which is not the case for patients whose hearing loss occurred before the acquisition of language. Finally, the findings confirm the key role of Broca’s area in restoration of speech perception, but only in individuals in whom Broca’s area has been active prior to the loss of hearing. 1. Introduction The cochlear implant (CI) transforms acoustic signals from the environment into electric impulses, which are then used to stimulate intact fibers of the auditory nerve. With this treatment, individuals with profound hearing loss (HL) are given the opportunity to gain or regain the sense of hearing. Current technology and speech processing strategies allow many CI recipients to achieve impressive accuracy in openset speech recognition, and the CI is arguably the most effective neural prosthesis ever developed [1–3]. However, the success of the outcome depends both on duration of deafness prior to implantation [4, 5] and on the onset of deafness before (prelingually) [4–7] or after (postlingually) [8] critical stages in the acquisition of language. In many cases, the greatest gains of performance occur in the first three months of use [9–11]. The dramatic improvements following implantation not only demonstrate the efficiency of the CI technology, but also point to the role of cortical plasticity as a means to reactivate brain function. Plasticity is a term used to describe the reorganization of the central nervous system by means of synaptic changes and rewiring of neural circuits. In cases of cochlear implantation, neural plasticity associated with deprivation of auditory input and adaptation to the absence of stimuli is of particular interest. Reduced input to the brain from impaired auditory pathways results in significant changes in the central auditory system [12] and is accompanied by a recruitment of deprived cortices in response to input from the intact senses [13–17]. When auditory input to the brain is reintroduced, this novel auditory experience may itself induce additional plasticity [18]. The sensory reafferentation provided by the CI thus offers a unique opportunity to study the effects of preceding deafness on functional brain organization. In normal-hearing (NH) adults, language processing is associated with extensive frontal activation in the left cerebral hemisphere, including the anterior (Brodmann’s Areas (BA) 45 and 47) and posterior (BA 44 and 45) parts of the left inferior frontal gyrus (LIFG), the latter often referred to 2 as Broca’s area [19, 20]. Traditionally, this area is mainly assigned an expressive language function, but several studies show a relationship between the perception of language and left frontal activity, both when stimuli are presented aurally [21–24] and visually [24–28]. Neuroimaging experiments comparing auditory responses of CI users and normalhearing control participants, while listening to speech or complex nonspeech, generally reveal bilateral activity in the primary and secondary auditory cortices, including both superior and middle temporal gyri [12, 29–34]. One consistent outcome of these studies is the more dominant right temporal activity of CI users listening to speech, that is, the observation of more bilateral activity than would be expected on the basis of the classical presumption of leftlateralized activity of language processing in normal-hearing [35]. However, in these studies, activation of other classic language regions such as Broca’s area was not a consistent finding. Naito and colleagues found Broca’s area to be activated only when the CI participants silently repeated sentences [31, 36]. Mortensen et al. [37] compared brain activity in experienced CI users according to their levels of speech comprehension performance. They found that, unlike CI users with low speech comprehension, single words and speech yielded raised activity in the left inferior prefrontal cortex (LIPC) in CI users with excellent speech perception. Some observed activations outside the classic language areas, including anterior cingulate, parietal regions, and left hippocampus, have been attributed to nonspecific attentional mechanisms and memory in CI users [31, 32]. Furthermore, some studies have reported convincing evidence of visual activity in response to auditory stimuli or auditory activity in response to visual stimuli in CI users. Although much debate about the identity of the brain systems that are changed and the mechanisms that mediate these changes exists, the general belief is that this cross-modal reorganization is associated with the strong visual speech-reading skills developed by CI users during the period of deafness, which are maintained or even improved after cochlear implantation, despite progressive recovery of auditory function [5, 11, 33, 38–41]. The possible reasons for these mixed results may include differences in experimental paradigms, small sample (...truncated)