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by Emily A. Tobey and Michael D. Devous, Sr.
Hearing scientists use neuroimaging techniques, which examine how the brain responds to external acoustic stimuli, to evaluate auditory processing. Investigators may probe how the brain responds to simple manipulations of frequency, intensity, or duration of the stimuli, or they may investigate how the brain responds to more complex listening conditions such as the appreciation of music, the sounds of familiar or unfamiliar languages, or the perception of speech signals in noise.
A growing literature focuses on learning how individuals with normal hearing or hearing loss process the sounds in their environment and the sounds needed to communicate. Two uses of neuroimaging techniques are in examining processes contributing to tinnitus and other annoying auditory conditions, and examining conditions in which an acoustic signal is transposed into an electrical stimulus such as a cochlear implant (CI). Several studies with individuals with cochlear implants concentrate on how the brain uses cortical resources to perceive speech or music. This information helps determine ways to improve the integrity of an electrical signal representing speech and to train people with cochlear implants to improve their listening performance.
Speech-perception performance in individuals [PDF] using cochlear implants varies greatly. Some individuals receive significant benefit when listening in both quiet and noisy situations, but others receive little benefit when listening in quiet environments. Individuals with severe-to-profound sensorineural hearing losses typically have a reduced number of intact hair cells within the cochlea which affects the status of the spiral ganglion cells and the transmission of information through the brainstem to the cortex. As a result, many individuals with sensorineural hearing loss experience "bottom-up" difficulties processing sound that are directly related to the anatomical and physiological condition of the peripheral auditory system.
Individuals with long-standing auditory deprivation related to sensorineural hearing loss also may experience "top-down" difficulties processing sounds. "Top-down" processing, in its most general form, refers to cognitive strategies used by listeners to decipher messages. For example, a listener might use the context of a sentence to fill in or guess the meaning of an unintelligible word in order to understand the complete sentence. For individuals using CIs, "top-down" processing may be evaluated through electrophysiological techniques or functional brain-imaging techniques (see sidebar on neuroimaging techniques, p. 8).
Neuroimaging studies with individuals who have cochlear implants use two major techniques, positron emission tomography (PET) and single photon emission computed tomography (SPECT), to examine cortical responses to speech perception tasks in individuals using cochlear implants. SPECT imaging of cortical responses to auditory signals in individuals being considered as candidates for cochlear implantation demonstrate drastically reduced responses that reflect limitations in the peripheral auditory system.
Studies indicate that the overall resting metabolism of persons with long-standing deafness differs from normal-hearing individuals. Elevated metabolic rates are associated with longer periods of auditory deprivation, as in the case of individuals with prelingual deafness, or with individuals who have less residual hearing. Individuals who are deaf demonstrate cortical responses to acoustic inputs that are characterized by a reduction in the extent and amount of activation in the primary and association auditory cortices. In determining candidacy for cochlear implantation, SPECT imaging may assist in determining the better ear for implantation by revealing the strongest, most intact pathway activated during auditory stimulation when all routine audiometric findings are equal across two ears.
Following cochlear implantation, cortical metabolism appears to be responsive to electrical stimulation, and alterations in cortical activations are observed in response to speech signals, pure tones, unfamiliar languages (such as a foreign language), and nonsense sounds. Our work and that of others demonstrate a reduction in the amount and extent of cortical activations observed in individuals before and after cochlear implantation relative to individuals with normal hearing. These reductions appear to reflect our inability to completely restore the peripheral auditory system to a level comparable to individuals with normal hearing. Individuals with a cochlear implant demonstrate greater responses in the primary and association cortices contralateral to the ear of implantation than observed before implantation.
The research suggests a strong relationship between the level of speech perception performance achieved with cochlear implantation and the activation patterns associated with primary auditory and auditory association cortices. High levels of speech perception after cochlear implantation are associated with bilateral activation of the primary auditory cortex (in Brodmann Areas 41, 42) and the auditory association cortex (Brodmann Areas 21, 22, and 38). However, low levels of speech perception after cochlear implantation are associated only with primary auditory cortex activation contralateral to the ear of implantation. These findings are consistent with the results of animal studies indicating that the auditory periphery, brainstem, and cortex are responsive to electrical stimulation from cochlear implants.
Enhancing Auditory Plasticity
A few studies use neuroimaging techniques to evaluate the "treatment" of the brain of individuals with a cochlear implant in order to maximize the potential of "top-down" processing. We were interested in determining how "plastic" or flexible the brains are of individuals who perform at low levels and with minimal activation patterns following cochlear implantation. One approach to examining how the minimal activation patterns could be enhanced is to provide a pharmacological stimulant [PDF] known to increase cortical activations during cognitive tasks in combination with clinical intervention. Our initial focus on improving "top-down" processing paired the administration of a pharmacological stimulant (d-amphetamine) with intensive audiologic/aural habilitation (AR). Adult cochlear implant users were randomly assigned to either a treatment group (d-amphetamine plus AR) or a control group (placebo plus AR). The AR program was held twice a week for 1.5 hours and featured sessions with similar content, although the level of sophistication of activities was designed to meet individual needs.
We examined auditory-only speech tracking before and after the eight-week intervention program. SPECT scans were collected at a similar time frame contrasting cortical activations produced when watching and listening to a reading versus watching only. Contrasting these conditions involves a technique that subtracts watching and listening from watching only, leaving only the listening responses.
Intensive AR with the placebo resulted in a gain of approximately 14% in auditory-only speech tracking scores. When AR was paired with d-amphetamine, however, auditory-only speech tracking scored showed gains of 43%. Prior to intervention, similar cortical activations were observed for both groups, but following the treatment program, the placebo group increased their activations bilaterally in the transverse and superior temporal gyri. The treatment group had substantially greater increased activations in the superior temporal gyrus ipsilateral to the ear implanted and more widespread activations contralateral to the ear of implantation, including in primary auditory and association-area cortices.
These initial observations are encouraging in two respects. First, they confirm that the brains of older individuals remain responsive to change guided by traditional AR or AR paired with pharmacological enhancement. Second, intervention outcomes are observable both in behavioral and objective measures of cortical activations. While promising, these observations also should be viewed with caution. We are only at the very initial stages of exploring how AR interfaces with changes in cortical activity. Many meticulous studies that carefully manipulate variables will be needed before these techniques can be considered for clinical use.
Emily A. Tobey is professor and Nelle C. Johnston Chair in Early Childhood Communication at the Callier Advanced Hearing Research Center of University of Texas at Dallas and adjunct professor in the departments of Radiology and Otolaryngology—Head and Neck Surgery, University of Texas Southwestern Medical Center. Contact her at etobey@utdallas.edu.
Michael D. Devous, Sr. is professor and associate director of the Nuclear Medicine Center, Department of Radiology, University of Texas Southwestern Medical Center, Dallas. Contact him at Michael.Devous@utsouthwestern.edu.
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