A sensitive period for cochlear implantation in deaf children

Introduction

Approximately 2 children per 1000 are born with sensorineural hearing loss. These children have varying degrees of deafness, and those who are at high risk of developing impaired speech and oral language, and who meet the candidacy criteria, are fitted with cochlear implants. A cochlear implant (CI) is a biomedical device that is surgically implanted in the cochlea of a deaf child and provides direct stimulation to the auditory nerve and brain. The electrical stimulation provided by the CI differs in principle from acoustic stimulation, however, it allows the implant recipient to differentiate speech sounds and interpret acoustic input in a meaningful manner, thereby facilitating the acquisition of speech and language. Worldwide there are approximately ~70,000 infants and children fitted with CIs.

During the first few years of life, the developing brain largely depends on external stimulation to form meaningful neural connections and a functional network, which can support behavioral learning (Hubel & Wiesel, 1970; Pallas, 2001). When sensory input such as hearing is absent, the consequences on brain development can be devastating. Animal studies have shown that deafness during the first few years of life significantly affects auditory cortical development, in that synaptogenesis (the creation of neuronal connections) and maturation of cortical layers is both delayed and abnormal (Klinke et al., 1999; Kral et al., 2000, 2001). The development of lower-level subcortical structures still occurs in deafness, but further development of neuronal connections and synaptic firing in the cortex is altered and later becomes non-existent as age increases (Klinke et al., 1999; Kral et al., 2000, 2001). In humans, similar results have been found using cortical auditory evoked potentials (CAEPs) via non-invasive electroencephalography (EEG) (Eggermont et al., 1997; Ponton et al., 1996). Normal auditory responses from the brain are either delayed or non-existent in deaf humans, indicating that brain maturation is highly dependent upon appropriate stimulation (Eggermont & Ponton, 2003). A cochlear implant can provide a deaf child with the stimulation necessary for the central auditory pathways to develop. As we will describe, cochlear implantation which occurs within a development time period of maximal neuronal plasticity, i.e., a sensitive period, results in the most optimal outcomes for the implanted child.

An important question in the field of deafness and cochlear implants is: When is the most optimal time to fit a young deaf child with a cochlear implant? In other words, at what age will implantation provide the best possibility for development of speech and language skills? In this review, we present evidence relating to a sensitive period for auditory brain development in cochlear implanted children and discuss consequences of implantation outside of the sensitive period relating to cortical re-organization.

A sensitive period for cochlear implantation

Sensitive periods in the cortex exist due to heightened levels of neuroplasticity. Neuroplasticity, or the ability of the brain to adapt in response to incoming sensory input, is quite high during the first few years of life, due in part to a major increase in synaptogenesis (Huttenlocher & Dabholkar, 1997). One way of examining the time limits for plasticity in the human central auditory system is the use of cortical auditory evoked potentials (CAEPs). In particular, the latency (time it takes for the brain to respond to stimulation) of the P1 component of the CAEP decreases systematically as a function of age. This decrease in latency is a result of the refinement and maturation of the central auditory pathways as the system develops. Synaptogenesis, pruning, and mylenation all contribute to this faster and more efficient transmission of sound (Eggermont & Ponton, 2003). Because the latency of the P1 peak decreases as age increases, this component of the CAEP acts as a biomarker of auditory cortical development.

The P1 response has been measured in deaf children who received CIs at different ages in order to examine the limits of plasticity in the central auditory system (Ponton et al., 1996; Sharma et al., 2002a, 2002b, 2002c, 2005a, 2005b, 2007, 2009; Sharma & Dorman 2006). Studies from our laboratory have examined P1 latency in 245 congenitally deaf children fit with a CI (Sharma et al., 2002a, 2002b, 2002c; Sharma & Dorman, 2006) and found that children who received stimulation via a CI early in childhood (<3.5 years) had normal P1 latencies within 6 months of implant use, while children who received CI stimulation late in childhood (>7 years) showed abnormal cortical response latencies even after years of implant use. A group of children receiving CIs between 3.5 and 7 years revealed highly variable response latencies. Overall, our P1 data suggest a sensitive period for optimal central auditory development of about 3.5 years in childhood. Though there is some variability in the data from ages 3.5 to 7 years, the sensitive period ends at approximately age 7 years. This finding of a sensitive period for central auditory development in humans is consistent with other studies of PET scan brain imaging in cochlear implanted children (Lee et al., 2001), evoked potential recordings (Eggermont & Ponton 2003) behavioral measures (Schorr et al., 2005) and from recordings in congenitally deaf animals (Kral et al, 2000; 2001; 2007 Ryugo et al., 1997). Speech and language studies have consistently shown that children implanted under age 3–4 years show significantly better speech and language skills than children implanted after 6–7 years (Geers, 2006; Kirk et al., 2002). In general, implantation at younger ages results in better speech and language outcomes for cochlear implanted children (Holt & Svirsky, 2008; Nicholas & Geers, 2007). As a result, in the United State Food and Drug Administration (FDA) has approved cochlear implantation at ~12 months of age.

Consequences of deafness beyond the sensitive period

A consequence of absent or significantly delayed auditory input to the brain is a re-organization between sensory systems (cross-modal re-organization). Thus, cochlear implantation within the sensitive period for auditory cortical development is critical not only for optimal speech and language development, but also to prevent re-organization of the cortex, which can limit the capacity for oral language learning. Animal studies suggest that at the end of the sensitive period the primary auditory cortex may be partially or completely disconnected (de-coupled) from surrounding higher-order cortex including language cortex (Kral, 2007). This leaves higher-order auditory cortex susceptible to recruitment from other sensory modalities. For example, in long-term deafened adults, it has been shown that visual and somatosensory processing may take place in auditory cortical areas (Buckley & Tobey, 2011; Finney et al., 2001; Neville et al., 1983; Sharma et al., 2007). Functionally, such cross-modal re-organization may result in enhanced processing for various aspects of the recruiting modality, as seen in greater attention to peripheral visual information in deaf individuals (Baverlier et al., 2000; Lomber et al., 2010; Neville & Lawson, 1987), while leaving significant deficits in auditory and multimodal processing, as seen in impaired auditory processing and auditory-visual integration (Gilley et al., 2010; Schorr et al., 2005).

Summary

Deafness and hearing loss during the first few years of life has negative consequences for the developing brain. Cochlear implantation bypasses the inner ear, providing direct stimulation to the central auditory pathways. Our studies show that the optimal time to implant a young deaf child is within a sensitive period of ~ age 3.5 years in childhood (best by the first two years of life). After the overall sensitive period ends (~ age 7 years), there is a high likelihood of de-coupling of primary cortical areas from surrounding higher-order cortex and subsequent cross-modal recruitment of the higher-order auditory cortical areas by other modalities such as vision and somatosensation. Thus, implantation within the sensitive period allows for normal auditory cortical maturation, providing ample opportunity for appropriate acquisition of speech and oral language.