Neurocognitive factors in sensory restoration of early deafness: a connectome model

Abstract

Progress in biomedical technology (cochlear, vestibular, and retinal implants) has led to remarkable success in neurosensory restoration, particularly in the auditory system. However, outcomes vary considerably, even after accounting for comorbidity-for example, after cochlear implantation, some deaf children develop spoken language skills approaching those of their hearing peers, whereas other children fail to do so. Here, we review evidence that auditory deprivation has widespread effects on brain development, affecting the capacity to process information beyond the auditory system. After sensory loss and deafness, the brain's effective connectivity is altered within the auditory system, between sensory systems, and between the auditory system and centres serving higher order neurocognitive functions. As a result, congenital sensory loss could be thought of as a connectome disease, with interindividual variability in the brain's adaptation to sensory loss underpinning much of the observed variation in outcome of cochlear implantation. Different executive functions, sequential processing, and concept formation are at particular risk in deaf children. A battery of clinical tests can allow early identification of neurocognitive risk factors. Intervention strategies that address these impairments with a personalised approach, taking interindividual variations into account, will further improve outcomes.

Figure 1:. Neurosensory restoration with prosthetic devices

Cochlear implants consist of internal (A, B) and external (A, C) components. The spiral ganglion and fibres of the auditory nerve (green, B) are the targets for stimulation, bypassing the non-functional organ of Corti (red, B). Activation of the implant generates an electrical response in selective auditory nerve fibres (B), which is carried to the auditory cortex (green, C) and interpreted as an auditory percept. The auditory cortex (C) is shown on the same side as the implant for illustrative purposes, but in reality the projection is mainly contralateral.

Figure 2:. Developmental events generating the brain’s connectome and auditory function

(A) Simplified sequence of selected human developmental processes depending on function and sensory input relative to onset of hearing and birth. (B) Schematic showing that functionality of the auditory system increases during development. Prenatal deafness (green) has the greatest effect on potential functionality. Congenital deafness (red) prevents many maturational steps. Early therapy (dotted lines) within the sensitive period can exploit juvenile plasticity and allows for large improvements in function. Late therapy (dashed lines) shows sufficient outcomes only with late onset of deafness (blue).

Figure 3:. Auditory component of the brain’s connectome in cats

Data taken from ref 15. Illustration of cortical anatomical connections in hearing cats (A) and congenitally deaf cats (B). The red dot (primary auditory field) depicts the area of placement of the dye to stain the connections. The strength of connections (black lines) is proportional to the line thickness. Ectopic connections (not found in hearing controls) are shown by red lines. The percentages represent the proportion compared with all connections of the given area. BA=Brodmann area.

Figure 4:. Auditory component of the human brain’s connectome

Illustration of interactions of the human auditory cortex with higher order areas involved in cognitive functions. Locations of the functions on the brain are schematic. Bottom-up connections are shown in green, top-down in red. The thickness of the lines does not reflect connection strength. The speech processor and the active cortex are shown on the same side of the brain for illustration purposes.

Figure 5:. Whisker plot of LEAF questionnaire findings in children with early cochlear implant and controls

Data taken from reference 47. Children with cochlear implants are shown in red and age-matched controls with normal hearing in blue. Individual datapoints are depicted as circles; dotted vertical lines show the range of the data (not including outliers beyond 99·3% of the whole population); the box depicts the IQR; the horizontal intersection line signifies the median; statistical outliers are marked by a cross. LEAF scores are raw scores based on sums of items as rated by parents. Scores range from 0 to 15 and are criteria-referenced, with 0–4 denoting no significant problem, 5–9 denoting a mild or borderline problem, and ≥10 denoting a problem in the area assessed by the LEAF subscale. LEAF=Learning, Executive, and Attention Functioning Scale. *Difference between controls and children with cochlear implant, p<0·05. †Difference between controls and children with cochlear implant, p<0·001.