Developmental neuroplasticity after cochlear implantation

Cortical development is dependent on stimulus-driven learning. The absence of sensory input from birth, as occurs in congenital deafness, affects normal growth and connectivity needed to form a functional sensory system, resulting in deficits in oral language learning. Cochlear implants bypass cochlear damage by directly stimulating the auditory nerve and brain, making it possible to avoid many of the deleterious effects of sensory deprivation. Congenitally deaf animals and children who receive implants provide a platform to examine the characteristics of cortical plasticity in the auditory system. In this review, we discuss the existence of time limits for, and mechanistic constraints on, sensitive periods for cochlear implantation and describe the effects of multimodal and cognitive reorganization that result from long-term auditory deprivation.

Introduction

When listening, the brain has to accomplish two functions: First, it has to analyze sound into acoustic features and represent those features that are essential for the differentiation of biologically important sounds. Second, it has to categorize these essential acoustic features into a representation (i.e. an auditory object) resistant to the inherent variability present in the sensory world. The representation of auditory objects is individual (subjective) and is critically dependent upon learning.

During learning, a sensory stimulus gains new behavioral significance, resulting in a dynamic reorganization of the representation of the features and objects associated with that sensory stimulus [1]. Receptive fields in the auditory cortex change after sufficient training 2, 3, 4, reflecting improvements in the performance of the learned task [5]. Both subcortical and cortical mechanisms contribute to this process. In the juvenile brain, the capacity for such plastic reorganization is greater 6, 7, 8, partly because of developmental changes in the molecular machinery of synaptic plasticity 9, 10. Such developmental periods of higher neuronal plasticity are called ‘sensitive periods’ [11]. Different sensitive periods exist for different behavioral functions [12], probably because of differences in underlying neuronal structures and functions and maturational rates 13, 14. Although most sensitive periods have an end-point after which learning is compromised, recent evidence suggests that some sensitive periods can be extended by certain sensory manipulations, such as long-term exposure to continuous non-patterned acoustic stimulation 15, 16. Thus, given high levels of juvenile plasticity, the existence of sensitive periods, and the dependence of postnatal development and learning on sensory experience 17, 18, an interesting question that arises is what are the effects of sensory deprivation on development? In this review, we explore the consequences of congenital deafness on auditory development and functioning.

Congenital deafness is frequent in humans (0.2–0.5 cases per 1000 live births) [19]. In profound sensorineural deafness, the human auditory nerve often survives the loss of inner ear hair cells 20, 21, 22 and is available to serve as a target for artificial (electrical) stimulation. Cochlear implants are devices that bypass a non-functional inner ear (organ of Corti) and provide direct stimulation to the auditory nerve. Electrical stimulation induces a pattern of activity that differs from acoustic stimulation, but which nonetheless, mimics the essential coding principles of the cochlea 23, 24. This allows most implant recipients to differentiate speech sounds and interpret auditory input [19]. There are approximately 200 000 cochlear implant users worldwide, including approximately 80 000 infants and children [19].

Children that become deaf before the development of language (i.e. prelingually deaf), if fitted with a cochlear implant early in childhood, demonstrate remarkable success in acquiring spoken language, especially if exposed to enriched language environments and supported by committed parents and caregivers 25, 26. However, implantation in later childhood results in successively less benefit 25, 26, and implantation in the elementary school age or later, as a rule, does not lead to good speech understanding 27, 28, 29, 30. Late-implanted subjects can detect the auditory stimulus (i.e. they hear), but the majority of them are not able to discriminate complex sounds appropriately in everyday situations, even after many years of implant use. The consequence is substantially compromised speech understanding and oral language learning.

Taken together, the differences in performance of early and late-implanted children demonstrate a sensitive period for cochlear implantation in early childhood. As we discuss in this review, neuronal mechanisms underlying sensitive periods can be explored in animal models (from cellular, synaptic to systems level), but, owing to the frequent clinical use of cochlear implants, such theories can also be directly investigated in the human brain. Therefore, the auditory system has developed into a model system for exploring the effects of sensory deprivation (and its subsequent restoration) with remarkably complementary results being observed across animal and human cochlear implant users. In this article, we review the evidence for the existence of a sensitive period for successful cochlear implantation, explore its underlying neural mechanisms, and describe the developmental and functional consequences when implantation occurs beyond this sensitive period.