Neural Plasticity in Cochlear Implants

The ability to hear consists of a complex sequence of physiological events. As sounds from the environment enter the ear, they travel through the ear canal and hit against the tympanic membrane. This pressure against the tympanic membrane then causes the oscicles (bones) of the middle ear to move. The stapes, the last in the sequence of middle ear bones, pushes against a fluid-filled window in the cochlea, which then vibrates the fluid inside. This vibration of fluid moves the structures in the cochlea, which stimulates the hair cells located within. The stimulation of hair cells sends an impulse to the auditory nerve. From the cochlea, the auditory nerve travels through the brainstem and up to Heschl’s gyrus, the primary auditory cortex, where sound is processed and analyzed. The impulse then travels further to Wernicke’s area where the signals are “interpreted into language-specific meaningful messages for the comprehension of spoken language” (Bhatnagar, 2008).

Damage at any point in this sequence can result in hearing loss. There are three main types of hearing loss: conductive, sensorineural, and mixed (which is a mixture of conductive and sensironeural). Conductive hearing loss is caused by damage to the outer or middle ear and affects sound transmission to the cochlea. A common form of conductive hearing loss in children is otitis media, or a middle ear infection, which occurs when fluid fills the middle ear and decreases the movement ability of the tympanic membrane and middle ear oscicles. In adults the most common form of conductive hearing loss is otosclerosis in which a bone growth restricts the stapes from moving. Conductive hearing loss is generally less severe than other types of hearing loss and is “characterized by fluctuating hearing loss, good word-speech recognition ability at high intensities, softly spoken speech, impaired auditory reflex, and an air bone gap” (Bhatnagar, 2008).

Sensorineural hearing loss is caused by damage to the hair cells in the cochlea or damage to the auditory nerve. Damage here can result from noise exposure, toxicity, degeneration, tumors, disease, etc. Sensorinerual hearing loss severity “can range from moderate to complete in the affected ear” and is characterized by “difficulty in understanding speech, particularly in noise and tinnitus” (Bhatnagar, 2008).

Some hearing can be restored in certain cases of sensorineural hearing loss through the use of a cochlear implant. This device contains a microprocessor, which separates the incoming sound into frequency, and an electrode, placed in the cochlea, which electrically stimulates the auditory nerve. Although some hearing is restored, the process of stimulation differs greatly from normal hearing physiology. In a cochlear implant, the dynamic range is “much less than that of the normal activation of auditory nerve fibers through excitation of inner hair cells”. In addition, the “randomness in the temporal firing is much less” and the “spread of excitation is much larger” in cochlear implants (Kral, 2006). Therefore, all people with cochlear implants must “learn to interpret this new input” (Kral, 2006).

Interpreting the input of a cochlear implant is even more complicated in people who are congenitally deaf and who have never heard. In these cases, the brain “has never learned to process the auditory information” and has reorganized as a result. In 1977, Rebillard found evidence to suggest a “possible reutilization of the cortical auditory areas deafferented from its primary modality”. More recent research has supported this theory, saying that “prelingual deafness results in partial reorganization of [the] cerebral cortex” (Wolff, 1990). Because of this reorganization, many support the theory of an early, critical period for the implantation of a cochlear implant.

Additional support for this critical period involves the early maturation of the auditory system and the evidence of synaptic deletion. Development of the cochlea is morphofunctionally complete at 24 weeks gestation and brainstem evoked responses have been “found in premature children” born at 28-29 weeks (Manrique, 1999). Additional development continues throughout the first 5 years of life as myelination occurs, and the auditory system matures. “The progressive changes in the auditory pathways and centers are to occur during the first 10 years of life, being especially dynamic in the first 5 years. In this particular period the human being has the most neuronal plasticity, or in other words the CNS has the greater ability to change the developmental pattern according to environmental influences” (Manrique, 1999).

If not stimulated, however, as in cases of congenital hearing loss, synaptic deletion can occur. Multiple studies have shown that removal of the cochlea results in loss of neural and cortical tissue associated with audition. Tierney, Russel, and Moore studied this effect in 1997 by removing the left cochlea in gerbils. They found statistically significant “whole nucleus volume reduction”, and a reduction in the “mean number of neurons” as a result. They concluded that there was “massive loss in CN [Cochlear Nucleus] neurons following deafferentation” (Tierney, 1997). Additional studies “observed a 14%-34% size decrease in neuronal somas” (Manrique, 1999) and others found an even greater “58% size decrease in neuronal somas within the CN” (Hashisaki, 1989) when the cochlea was removed. These studies support the “use it or loose it” theory that suggests that cortical and subcortical tissue not used during the critical years of development will die or be reassigned to other processes.

So, if deafferentation and reorganization occur as a result of hearing loss, can cochlear implants re-teach the brain to use the changed cortical tissue or prevent the changes from occurring all together? Born and Rubel (1988) found that “the effects of denervating muscles can be largely reversed by direct electrical stimulation”. Leak (1999) also found this to be true within the spiral ganglion (SG) of kittens. Their research suggested “a 20% difference in density” in the SG cell somata between stimulated and non-stimulated ears, and showed cells “were significantly larger in the stimulated ears”. This indicates that if implanted early enough, synaptic deletion can be curbed and the brain can learn to process and use the incoming electrical-auditory stimuli.
Although the brain learns to use the stimuli, research continues to suggest that the brain reorganizes to accommodate for the changes in stimulation after implantation. One such study states that “postlingually deaf subjects learn the meaning of sounds after cochlear implantation by forming new associations between sound and their sources” (Giraud, 2001b). Giraud, Price, Graham, and Frackowiak (2001a) investigated this subject by looking at the involvement of the visual cortex in auditory language tasks after cochlear implantation. They used PET scans to examine the cortical activity of 12 subjects and found that all showed “significant activation of [the] visual cortex” (Giraud, 2001a). Specifically, the calcarine sulcus and lingual gyrus were active during these tasks. This activation was not present in the control group of normal hearing individuals.

Ponton and Eggermont found differences in auditory evoked potentials between people with cochlear implants and normal hearing individuals. Specifically, they found differences in P1 latencies, which measure the delay in synaptic propagation through the auditory pathway. They observed “prolonged P1 latencies compared to age-matched normal-hearing peers” and specifically found “a delayed maturation nearly equivalent to the period of deafness” (Ponton, 2001).

Sharma, Dorman, and Kral found similar differences in their 2005 study when they looked at the P1 latencies of early (before age 3.5) and late (after age 7) implanted, congenitally deaf children. They found that “both early- and late- implanted children showed a 35% decrease in P1 latencies in the initial month after implantation”, but after that they found “significantly different P1 latency” between early and late implanted groups (Sharma, 2005). In a study prior to that, Sharma, Dorman, and Sphar (2002) found that in children implanted at age “11 or older”, there was “very litte or no change in P1 latency after 1 to 2 years of electrical stimulation”. Children implanted by age 7 however, showed decreases in P1 latency “within a year of implantation”, and “children implanted before age 3.5” were found to have “very large decreases in latency within the first several months after the switch on” (Sharma, 2002).

These studies suggest that age of implantation significantly affects auditory pathway maturation and that, if implanted early, children can have latencies “within normal limits”(Sharma, 2005). They also support the theory of a ‘critical period’ in which the “auditory system appears maximally plastic” and therefore, the neural adaption to the cochlear implant is greatest.

Other reasons for early implantation involve the early development of language and the critical period associated with language acquisition. Studies have looked at the effect of early implantation on language and have shown a “rapid improvement in speech production and language acquisition after improved speech perception through a cochlear implant for these children implanted before 5 years of age” (Brackett, 1998). More specifically, children showed an increase in their receptive and expressive vocabulary and in sentence length and complexity in the first year after implantation, if implanted before 5 (Brackett, 1998).

Contrary studies have disputed the theory of a critical period, offering the opinion that all benefit from implantation and that it is “unlikely one critical period” exists (Harrison, 2005). They also discuss the biasness of the outcome measurement tool and that the measured behavioral outcome is “often the result of many mechanisms, each with a differing developmental dynamic” (Harrison, 2005). Even though these authors question a strict critical period, they admit there is an “age related plasticity effect”, and that “cochlear implant intervention at an early age in the congenitally deaf infant results in significantly better outcomes in speech understanding and language development” (Harrison, 2005).

In addition to age, Kral and Tellein (2006) suggest other factors that affect the outcome of the cochlear implant. “Peripheral Factors” include the “cochlear implant processor, the electrode type, its position and extent within the cochlea, pattern of degeneration in the auditory nerve” and the “status of myelination of the auditory nerve”. The other group of “Central Factors” includes the “status of the central auditory system (congenital, pre/postlingual deafness), it’s plasticity (age), and subjective cognitive factors that determine how effectively the subject adapts to the new type of sensory input.”

Although all of these factors are important, high neural plasticity may be the most pivotal of the central factors, as time of implantation can often be controlled. As suggested by many different studies, early cochlear implantation can decrease synaptic deletion, alter neural activity, and increase speech and language abilities. For all of these reasons, it is important children be implanted at an early age if the cochlear implant team, which includes the family, decides it is appropriate for the individual child.

References

Bhatnagar, S. C. (2008). Neuroscience: for the Study of Communicative Disorders (3rd ed.). Baltimore, MD: Lippincott Williams & Wilkins, a Wolters Kluwer business.

Born, D.E., & Rubel, E.W. (1988). Afferent Influences on Brain Stem Auditory Nuclei of the Chicken: Presynaptic Action Potentials Regulate Protein Synthesis in Nucleus Magnocellularis Neurons. The Journal of Neuroscience, 8, 901-919.

Brackett, D., & Zara, C. V. (1998). Communication Outcomes Related to Early Implantation. The American Journal of Otology, 19, 453-460.

Giraud, A., Price, C.J., Graham, J.M., & Frackowiak, R.S.J. (2001a). Functional Plasticity of Language-Related Brain Areas after Cochlear Implantation. Brain 2001, 124, 1307-1316.

Giraud, A., Price, C.J., Graham, J.M., Truy, E., & Frackowiak, R.S.J. (2001b). Cross-Modal Plasticity Underpins Language Recovery after Cochlear Implantation. Neuron, 30, 657-663.

Harrison, R.V., Gordon, K.A., & Mount, R.J. (2005). Is There a Critical Period for Cochlear Implantation in Congenitally Deaf Children? Analyses of Hearing and Speech Perception Performance after Implantation. Wiley Periodicals, Inc. Developmental Psychobiology, 46, 252-261.

Hashisaki, G.T., & Rubel, E.W. (1989) Effects of Unilateral Cochlea Removal on Anteroventral Cochlear Nucleus Neurons in Developing Gerbils. The Journal of Comparative Neurology, 283, 465-473.

Kral, A., Tillein, J. (2006). Brain Plasticity under Cochlear Implant Stimulation. Advances in Oto-Rhino-Laryngology, 64, 89-108.

Leake, P.A., Hradek, G.T., & Snyder, R.L. (1999). Chronic Electrical Stimulation by a Cochlear Implant Promotes Survival of Spiral Ganglion Neurons after Neonatal Deafness. The Journal of Comparative Neurology, 412, 543-562.

Manrique, M., Cervera-Paz, F.J., Huarte, A., Perez, N., Molina, M., & Garcıa-Tapia, R. (1999). Cerebral Auditory Plasticity and Cochlear Implants. International Journal of Pediatric Otorhinolaryngology, 49, 193-197.

Ponton, C.W., & Eggermont, J.J. (2001). Of Kittens and Kids: Altered Cortical Maturation following Profound Deafness and Cochlear Implant Use. Audiology & Neoro-Otology, 6, 363-380.

Rebillard, G., Carlier, E., Rebillard, M., & Pujol, R. (1977). Enhancement of Visual Responses on the Primary Auditory Cortex of the Cat after an Early Destruction of Cochlear Receptors. Brain Research, 129, 162-164.

Sharma, A., Dorman, M.F., & Kral, A. (2005). The Influence of a Sensitive Period on Central Auditory Development in Children with Unilateral and Bilateral Cochlear Implants. Hearing Research, 203, 134-143.

Sharma, A., Dorman, M.F., & Spahr, A.J. (2002). A Sensitive Period for the Development of the Central Auditory System in Children with Cochlear Implants: Implications for Age of Implantation. Ear and Hearing, 23, 532-539.

Tierney, T.S., Russell, F.A., & Moore, D.R. (1997). Susceptibility of Developing Cochlear Nucleus Neurons to Deafferentation-Induced Death Abruptly Ends Just Before the Onset of Hearing. The Journal of Comparative Neurology, 378, 295-306.

Wolff, A.B., & Thatcher, R.W., (1990). Cortical Reorganization in Deaf Children. Journal of Clinical and Experimental Neuropsychology, 12, 209-221.