Cortical reorganization in children with cochlear implants

Abstract

Congenital deafness leads to atypical organization of the auditory nervous system. However, the extent to which auditory pathways reorganize during deafness is not well understood. We recorded cortical auditory evoked potentials in normal hearing children and in congenitally deaf children fitted with cochlear implants. High-density EEG and source modeling revealed principal activity from auditory cortex in normal hearing and early implanted children. However, children implanted after a critical period of seven years revealed activity from parietotemporal cortex in response to auditory stimulation, demonstrating reorganized cortical pathways. Reorganization of central auditory pathways is limited by the age at which implantation occurs, and may help explain the benefits and limitations of implantation in congenitally deaf children.

Introduction

Development and organization of sensory pathways in the cortex is dependent on sensory experience. A lack of sensory input, such as in deafness, impedes the normal growth and early connectivity needed to form a functional sensory system — in some cases irretrievably (Wiesel and Hubel, 1965). Evidence from animal models of congenital deafness has revealed abnormal formation of auditory nerve fibers that terminate in the lower brainstem (Lee et al., 2003, Ryugo et al., 2005). Other animal models have shown reduced synaptic activity in the sensory deprived auditory cortex in response to acute electrical stimulation (Kral et al., 2002). In layer specific recordings from auditory cortex in congenitally deaf cats, supragranular layers showed less synaptic activity with decreased response amplitudes and increased response latencies compared to normal-hearing cats, while infragranular layers showed very little synaptic activity at all (Kral et al., 2000). Moreover, the synaptic currents had significantly reduced sink amplitudes, suggesting deficient corticothalamic and corticocortical projections. The reduced responsiveness of these physiological mechanisms may be due to a deterioration of the supporting anatomical structures during deprivation, to a reorganization of those structures, or to a combination thereof.

In humans, the cortical auditory evoked potential (CAEP) provides information about maturation of auditory pathways terminating in auditory cortex, and reflects recurrent cortical activity mediated by corticothalamic loops (Eggermont, 1992, Kral et al., 2000). These recurrent loops mediate subsequent corticocortical projections (Winguth and Winer, 1986) that may be disrupted after auditory deprivation. Restoring function to these modulatory projections may be possible with cochlear implantation, as long as the central auditory system (CAS) remains maximally plastic and the effects of degeneration have not completely taken effect. Indeed, evidence from animal data reported by Klinke et al. (1999) have found that at least some deprivation effects can be reversed with chronic electrical stimulation to the auditory pathways. However, while early-implantation in a maximally plastic CAS restores maturation of the auditory pathways, providing auditory input after prolonged deprivation may not initiate stimulus driven reorganization with the same success.

The latency of the P1 CAEP has been used to examine CAS maturation in children with cochlear implants. Sharma et al., 2002a, Sharma et al., 2002b, Sharma et al., 2002c and Ponton et al. (1996) examined P1 latencies in children with CIs and revealed prolonged latencies compared to normal-hearing children. Further analysis revealed that P1 latency appears to continue a developmental progression after implantation. Moreover, Sharma et al., 2002a, Sharma et al., 2002b, Sharma et al., 2002c showed that age of implantation was a critical factor in P1 latency maturation. Children implanted after age 7 years did not show age appropriate P1 latencies, while children implanted prior to age 3.5 years showed P1 latencies within the normal developmental limits. Further examinations of P1 latencies in children with CIs compared to a group of age-matched normal-hearing peers, revealed no significant differences in P1 latency between the early-implanted and normal hearing children (Sharma et al., 2002a). Collectively, these data suggest a sensitive period of about 3.5 years for which auditory stimulation is necessary to promote normal maturation of the CAS as revealed by the P1 CAEP.

Children who are implanted after the age of seven years almost always show evidence of abnormal central auditory maturation when examining the latency of the P1 response (Sharma and Dorman, 2006, Sharma et al., 2002b, Sharma et al., 2005). However, if implantation occurs very early in childhood, then the P1 latency will typically follow a normal developmental trajectory (Sharma et al., 2002a, Sharma et al., 2002b). Furthermore, it is well established that the earlier in life a deaf child receives a cochlear implant, the better their development of natural language skills (Colletti et al., 2005, Connor et al., 2006, Francis and Niparko, 2003, Kang et al., 2004, Kirk et al., 2002). Taken together, these results support the conventional wisdom that early stimulation is necessary to support normal sensory development. Understanding the physiological mechanisms associated with both normal and abnormal sensory development may help us better understand and plan for successful rehabilitation in children with cochlear implants.

There is evidence from animal and human studies to suggest at least some level of cross-modal reorganization from one sensory modality when another modality is deprived of input (Armstrong et al., 2002, Doron and Wollberg, 1994, Lee et al., 2001, Yaka et al., 2000). Restoring auditory input to a reorganized system may mean that functional access to the cortex is limited to those pathways still available after a prolonged period of deprivation. It is likely that the time course of deterioration and reorganization of the deprived auditory pathways limits the success of restoring auditory input with a cochlear implant (CI). Therefore, restoring input very early to a highly plastic auditory system will likely lead to an improved chance of typical auditory function.

In research reported here, we used current source reconstruction and dipole source analyses derived from high density EEG recordings to estimate generators for the P1 response in three groups of children: Normal hearing children, congenitally deaf children who received a cochlear implant before the age of four years, and congenitally deaf children who received a cochlear implant after the age of seven years. At issue was whether cortical organization as reflected by the generators of the P1 response was the same for the three groups of listeners.