ReviewCochlear implants and brain plasticity
Introduction
Worldwide, over 110,000 deaf adult and children benefit from direct electrical stimulation of their AN via a cochlear implant. Implant recipients exhibit a wide range of speech perception skills with a range of factors identified as affecting clinical performance (Blamey et al., 1996). The level of performance of pre-linguistically deaf adults generally remains well below that of post-linguistically deaf adults (Busby and Clark, 1999, Busby et al., 1993, Eddington et al., 1978). It is remarkable that the best patients can exhibit near-normal open-set speech perception, at least in a quiet environment, given the abnormal (and in many ways impoverished) input provided by these devices. The importance of auditory experience in the clinical performance of cochlear implant users has been consistently emphasized (Blamey et al., 1996, Gantz et al., 1993, Rubinstein et al., 1999). Clearly, changes within the auditory system underlie some of the improvements in speech perception seen in implant patients with device use, although it has not been established whether the improvements are mediated by changes in auditory cortex per se.
The capacity for plasticity in the response properties of neurons in, and consequently the functional organization of, cortical and sub-cortical sensory structures was generally believed to be maximal within ‘critical periods’ during early development (Hensch, 2004). It was believed that changes in experience during these early periods – when neuronal pathways and connections were being formed – but not later in life could drive changes in sensory processing mechanisms. However, the capacity for plasticity in adult sensory systems, given appropriate patterns of behaviourally significant input, has more recently become generally accepted (for review see Kaas and Florence, 2001) and confirmed in the auditory system (for reviews see Irvine, 2007, Weinberger, 2007).
The effects of restrictions in output from the cochlea, in both immature and adult animals, on the tonotopic organisation (for review see Irvine and Wright, 2005) and the temporal processing ability (Bao et al., 2004), of the thalamo-cortical auditory system have been well characterised. Less well studied are the effects of chronic, behaviourally relevant, electrical stimulation of the AN – similar to that used in cochlear implants – on cochleotopic organisation and temporal processing.
Complicating the interpretation of plasticity in the auditory cortex produced by such stimulation is that there are many changes consequent on a sensorineural hearing loss that almost invariably precede the chronic stimulation (for review see Shepherd et al., 2006). These changes include: significant reduction in spiral ganglion neurons; de-myelination of residual spiral ganglion neuron soma and possibly part of their central processes; shrinkage of the perikaryon of neurons throughout the auditory pathway; and reduced spontaneous activity throughout the auditory pathway. As many of the changes associated with sensorineural hearing loss are ‘down-stream’ from the cortex in the auditory pathway, they affect the input, and the organization of that input, into the auditory cortex. This problem of interpretation due to down-stream changes is equally true of changes associated with chronic stimulation.
It is also important to note that not all changes in neural responsiveness and organization are necessarily plastic in nature, as some changes can be explained as passive consequences of the altered input. For example, the frequency tuning of AN fibres, and consequently of neurons throughout the auditory pathway, is immediately altered after destruction of the outer hair cells (Dallos and Harris, 1978). It is also not always a simple matter to distinguish between plastic and non-plastic changes (Calford, 2002, Irvine and Wright, 2005). However, we will define plasticity as involving some form of active or dynamic modification of neural properties resulting from the altered input.
This paper will review the evidence of plastic changes in the central auditory system resulting from chronic electrical stimulation of the AN, with an emphasis on behaviourally relevant stimulation. First, evidence from animal studies focussing on the response properties of neurons in, and the functional organization of, the primary auditory cortex (AI) will be reviewed. Second, electrophysiological and functional imaging studies of the auditory cortex in cochlear implant patients will be reviewed. Finally, the relationship between the reported changes in the auditory cortex and psychophysical studies of both pitch and speech perception will be discussed.
Section snippets
Basic response properties
Individual neurons within layer III/IV of AI of normal hearing (or acutely deafened) cats have well characterized input–output functions for electrical stimulation (Hartmann et al., 1997, Popelar et al., 1995, Raggio and Schreiner, 2003, Schreiner and Raggio, 1996). Neurons exhibit either monotonic (∼55%) or non-monotonic input–output functions, with dynamic ranges of approximately 10 dB, and minimum first spike latencies of around 8 ms. Cortical field potentials exhibit both a short- (<80 ms) and
Electrophysiology
Evidence from clinical studies of the P1 evoked cortical potential indicates that there is a sensitive period, ending around 3.5 years of age, during which the human central auditory pathway is maximally plastic (Eggermont and Ponton, 2003, Ponton and Eggermont, 2001, Ponton et al., 1996, Sharma et al., 2002). Children who receive effective cochlear stimulation within this period develop electrically evoked cortical potentials with latencies (∼100 ms) that reach those of aged-matched
Conclusion
A growing body of functional imaging and psychophysical studies in humans and predominantly neurophysiological studies in animals is providing further evidence for plasticity in the central auditory pathway. It is clear that genetic cues are sufficient to generate a basic framework, with the development of at least a rudimentary pathway in the absence of any auditory experience, which is sufficient to provide both the temporal and spatial cues necessary for speech perception using a cochlear
Acknowledgement
The authors’ research is supported by the National Institute of Deafness and Communication Disorders of the USA (N01-DC-3-1005).
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