Cochlear implantation after traumatic brain injury without otic capsule fracture: A case report and literature review.

OBJECTIVE: The aim of this study was to report a case of cochlear implantation (CI) for a patient with an otic capsule-sparing traumatic brain injury (TBI) and to review the relevant literature. METHODS: A patient with history of TBI received a CI for bilateral profound hearing loss. A systematic review of the literature was performed to identify and compare similar cases. RESULTS: A 36-year-old male with a history of hearing loss from right acute labyrinthitis was referred for bilateral profound sensorineural hearing loss (SNHL) after a fall with associated injury to the central auditory nervous system (CANS) including the brainstem. On the right, behavioral acoustic threshold measurements were in the profound range with absent OAEs. On the left, testing revealed no measurable behavioral acoustic thresholds and variable physiologic measures. A right unilateral cochlear implant was performed with most recent follow-up demonstrating speech awareness thresholds of 25 dB HL with excellent detection of all 6 Ling sounds. However, the patient also continues to suffer from other neurologic sequelae related to his TBI, which challenge his ability to demonstrate objective and subjective benefit. A systematic review of the literature demonstrates variable outcomes for patients with TBI and SNHL. CONCLUSIONS: Patients with profound SNHL and TBI present a distinct rehabilitative challenge for clinicians. CI may provide meaningful benefit in this population, though care should be taken in patient selection and counseling.

Blast Exposure Disrupts the Tonotopic Frequency Map in the Primary Auditory Cortex.

Blast exposure can cause various auditory disorders including tinnitus, hyperacusis, and other central auditory processing disorders. While this is suggestive of pathologies in the central auditory system, the impact of blast exposure on central auditory processing remains poorly understood. Here we examined the effects of blast shockwaves on acoustic response properties and the tonotopic frequency map in the auditory cortex. We found that multiunits recorded from the auditory cortex exhibited higher acoustic thresholds and broader frequency tuning in blast-exposed animals. Furthermore, the frequency map in the primary auditory cortex was distorted. These changes may contribute to central auditory processing disorders.

Auditory-cortex lesions impair contralateral tone-pattern detection under informational masking.

Impaired hearing contralateral to unilateral auditory-cortex lesions is typically only observed under conditions of perceptual competition, such as dichotic presentation or speech in noise. It remains unclear, however, if the source of this effect is direct competition in frequency-specific neurons, or if enhanced processing load in more distant frequencies can also impair auditory detection. To evaluate this question, we studied a group of patients with unilateral auditory-cortex lesions (N = 14, six left-hemispheric (LH), eight right-hemispheric (RH); four females; age range 26-72 years) and a control group (N = 25; 15 females; age range 18-76 years) with a target-detection task in presence of a multi-tone masker, which can produce informational masking. The results revealed reduced sensitivity for monaural target streams presented contralateral to auditory-cortex lesions, with an approximately 10% higher error rate in the contra-lesional ear. A general, bilateral reduction of target detection was only observed in a subgroup of patients, who were classified as additionally suffering from auditory neglect. These results demonstrate that auditory-cortex lesions impair monaural, contra-lesional target detection under informational masking. The finding supports the hypothesis that neural mechanisms beyond direct competition in frequency-specific neurons can be a source of impaired hearing under perceptual competition in patients with unilateral auditory-cortex lesions.

Ablation of the auditory cortex results in changes in the expression of neurotransmission-related mRNAs in the cochlea.

The auditory cortex (AC) dynamically regulates responses of the Organ of Corti to sound through descending connections to both the medial (MOC) and lateral (LOC) olivocochlear efferent systems. We have recently provided evidence that AC has a reinforcement role in the responses to sound of the auditory brainstem nuclei. In a molecular level, we have shown that descending inputs from AC are needed to regulate the expression of molecules involved in outer hair cell (OHC) electromotility control, such as prestin and the α10 nicotinic acetylcholine receptor (nAchR). In this report, we show that descending connections from AC to olivocochlear neurons are necessary to regulate the expression of molecules involved in cochlear afferent signaling. RT-qPCR was performed in rats at 1, 7 and 15 days after unilateral ablation of the AC, and analyzed the time course changes in gene transcripts involved in neurotransmission at the first auditory synapse. This included the glutamate metabolism enzyme glutamate decarboxylase 1 (glud1) and AMPA glutamate receptor subunits GluA2-4. In addition, gene transcripts involved in efferent regulation of type I spiral ganglion neuron (SGN) excitability mediated by LOC, such as the α7 nAchR, the D2 dopamine receptor, and the α1, and γ2 GABAA receptor subunits, were also investigated. Unilateral AC ablation induced up-regulation of GluA3 receptor subunit transcripts, whereas both GluA2 and GluA4 mRNA receptors were down-regulated already at 1 day after the ablation. Unilateral removal of the AC also resulted in up-regulation of the transcripts for α7 nAchR subunit, D2 dopamine receptor, and α1 GABAA receptor subunit at 1 day after the ablation. Fifteen days after the injury, AC ablations induced an up-regulation of glud1 transcripts.

Encoding and retrieval of artificial visuoauditory memory traces in the auditory cortex requires the entorhinal cortex.

Damage to the medial temporal lobe impairs the encoding of new memories and the retrieval of memories acquired immediately before the damage in human. In this study, we demonstrated that artificial visuoauditory memory traces can be established in the rat auditory cortex and that their encoding and retrieval depend on the entorhinal cortex of the medial temporal lobe in the rat. We trained rats to associate a visual stimulus with electrical stimulation of the auditory cortex using a classical conditioning protocol. After conditioning, we examined the associative memory traces electrophysiologically (i.e., visual stimulus-evoked responses of auditory cortical neurons) and behaviorally (i.e., visual stimulus-induced freezing and visual stimulus-guided reward retrieval). The establishment of a visuoauditory memory trace in the auditory cortex, which was detectable by electrophysiological recordings, was achieved over 20-30 conditioning trials and was blocked by unilateral, temporary inactivation of the entorhinal cortex. Retrieval of a previously established visuoauditory memory was also affected by unilateral entorhinal cortex inactivation. These findings suggest that the entorhinal cortex is necessary for the encoding and involved in the retrieval of artificial visuoauditory memory in the auditory cortex, at least during the early stages of memory consolidation.

Fear conditioning enhances γ oscillations and their entrainment of neurons representing the conditioned stimulus.

Learning alters the responses of neurons in the neocortex, typically strengthening their encoding of behaviorally relevant stimuli. These enhancements are studied extensively in the auditory cortex by characterizing changes in firing rates and evoked potentials. However, synchronous activity is also important for the processing of stimuli, especially the relationship between gamma oscillations in the local field potential and spiking. We investigated whether tone/shock fear conditioning in rats, a task known to alter responses in auditory cortex, also modified the relationship between gamma and unit activity. A boost in gamma oscillations developed, especially at sites tuned near the tone, and strengthened across multiple conditioning sessions. Unit activity became increasingly phase-locked to gamma, with sites tuned near the tone developing enhanced phase-locking during the tone, whereas those tuned away maintained a tendency to decrease their phase-locking. Enhancements in the coordination of spiking between sites tuned near the tone developed within the first conditioning session and remained throughout the rest of training. Enhanced cross-covariances in unit activity were strongest for subjects that exhibited robust conditioned fear. These results illustrate that changes in sensory cortex during associative learning extend to the coordination of neurons encoding the relevant stimulus, with implications for how it is processed downstream.

Losing the sound of concepts: damage to auditory association cortex impairs the processing of sound-related concepts.

Conceptual knowledge is classically supposed to be abstract and represented in an amodal unitary system, distinct from the sensory and motor brain systems. A more recent embodiment view of conceptual knowledge, however, proposes that concepts are grounded in distributed modality-specific brain areas which typically process sensory or action-related object information. Recent neuroimaging evidence suggested the significance of left auditory association cortex encompassing posterior superior and middle temporal gyrus in coding conceptual sound features of everyday objects. However, a causal role of this region in processing conceptual sound information has yet to be established. Here we had the unique chance to investigate a patient, JR, with a focal lesion in left posterior superior and middle temporal gyrus. To test the necessity of this region in conceptual and perceptual processing of sound information we administered four different experimental tasks to JR: Visual word recognition, category fluency, sound recognition and voice classification. Compared with a matched control group, patient JR was consistently impaired in conceptual processing of sound-related everyday objects (e.g., "bell"), while performance for non-sound-related everyday objects (e.g., "armchair"), animals, whether they typically produce sounds (e.g., "frog") or not (e.g., "tortoise"), and musical instruments (e.g., "guitar") was intact. An analogous deficit pattern in JR was also obtained for perceptual recognition of the corresponding sounds. Hence, damage to left auditory association cortex specifically impairs perceptual and conceptual processing of sounds from everyday objects. In support of modality-specific theories, these findings strongly evidence the necessity of auditory association cortex in coding sound-related conceptual information.

Dissociation of detection and discrimination of pure tones following bilateral lesions of auditory cortex.

It is well known that damage to the peripheral auditory system causes deficits in tone detection as well as pitch and loudness perception across a wide range of frequencies. However, the extent to which to which the auditory cortex plays a critical role in these basic aspects of spectral processing, especially with regard to speech, music, and environmental sound perception, remains unclear. Recent experiments indicate that primary auditory cortex is necessary for the normally-high perceptual acuity exhibited by humans in pure-tone frequency discrimination. The present study assessed whether the auditory cortex plays a similar role in the intensity domain and contrasted its contribution to sensory versus discriminative aspects of intensity processing. We measured intensity thresholds for pure-tone detection and pure-tone loudness discrimination in a population of healthy adults and a middle-aged man with complete or near-complete lesions of the auditory cortex bilaterally. Detection thresholds in his left and right ears were 16 and 7 dB HL, respectively, within clinically-defined normal limits. In contrast, the intensity threshold for monaural loudness discrimination at 1 kHz was 6.5 ± 2.1 dB in the left ear and 6.5 ± 1.9 dB in the right ear at 40 dB sensation level, well above the means of the control population (left ear: 1.6 ± 0.22 dB; right ear: 1.7 ± 0.19 dB). The results indicate that auditory cortex lowers just-noticeable differences for loudness discrimination by approximately 5 dB but is not necessary for tone detection in quiet. Previous human and Old-world monkey experiments employing lesion-effect, neurophysiology, and neuroimaging methods to investigate the role of auditory cortex in intensity processing are reviewed.

[The role of the auditory cortex in the spatial information processing]. / La corteza auditiva en el procesamiento de la informacion espacial.

Sound localization is a computational process accomplished along the auditory pathway. Once the acoustic information received at each ear is analyzed independently (monaural cues) and comparatively (binaural cues), those cues are integrated to generate a coherent spatial percept. Using adult ferrets trained by positive conditioning in a spatial task, we aimed to study the role of the auditory cortex in the ability to localize sounds under both normal hearing and monaurally occluded conditions, the latter of which requires a reinterpretation of the values of the localization cues. Sound localization deficits were found after lesion or inactivation of the different auditory cortical regions, thereby indicating their participation in spatial processing. The differential impairments found in the approach-to-target and in the head movement responses reveal the complex relationship between cortex and midbrain which are putatively responsible for the voluntary and reflexive aspects of localization behaviour respectively. Furthermore, every auditory cortical region contributes to the adaptation process that follows monaural occlusion, indicating the key role that the auditory cortex plays in experience-dependent plasticity. Also, the selective lesion of the descending projections from the auditory cortex to the inferior colliculus by chromophore-targeted laser photolysis has revealed the essential function that descending pathways play in learning-induced localization plasticity.

Discrimination of brief speech sounds is impaired in rats with auditory cortex lesions.

Auditory cortex (AC) lesions impair complex sound discrimination. However, a recent study demonstrated spared performance on an acoustic startle response test of speech discrimination following AC lesions (Floody et al., 2010). The current study reports the effects of AC lesions on two operant speech discrimination tasks. AC lesions caused a modest and quickly recovered impairment in the ability of rats to discriminate consonant-vowel-consonant speech sounds. This result seems to suggest that AC does not play a role in speech discrimination. However, the speech sounds used in both studies differed in many acoustic dimensions and an adaptive change in discrimination strategy could allow the rats to use an acoustic difference that does not require an intact AC to discriminate. Based on our earlier observation that the first 40 ms of the spatiotemporal activity patterns elicited by speech sounds best correlate with behavioral discriminations of these sounds (Engineer et al., 2008), we predicted that eliminating additional cues by truncating speech sounds to the first 40 ms would render the stimuli indistinguishable to a rat with AC lesions. Although the initial discrimination of truncated sounds took longer to learn, the final performance paralleled rats using full-length consonant-vowel-consonant sounds. After 20 days of testing, half of the rats using speech onsets received bilateral AC lesions. Lesions severely impaired speech onset discrimination for at least one-month post lesion. These results support the hypothesis that auditory cortex is required to accurately discriminate the subtle differences between similar consonant and vowel sounds.

Auditory and cognitive deficits associated with acquired amusia after stroke: a magnetoencephalography and neuropsychological follow-up study.

Acquired amusia is a common disorder after damage to the middle cerebral artery (MCA) territory. However, its neurocognitive mechanisms, especially the relative contribution of perceptual and cognitive factors, are still unclear. We studied cognitive and auditory processing in the amusic brain by performing neuropsychological testing as well as magnetoencephalography (MEG) measurements of frequency and duration discrimination using magnetic mismatch negativity (MMNm) recordings. Fifty-three patients with a left (n = 24) or right (n = 29) hemisphere MCA stroke (MRI verified) were investigated 1 week, 3 months, and 6 months after the stroke. Amusia was evaluated using the Montreal Battery of Evaluation of Amusia (MBEA). We found that amusia caused by right hemisphere damage (RHD), especially to temporal and frontal areas, was more severe than amusia caused by left hemisphere damage (LHD). Furthermore, the severity of amusia was found to correlate with weaker frequency MMNm responses only in amusic RHD patients. Additionally, within the RHD subgroup, the amusic patients who had damage to the auditory cortex (AC) showed worse recovery on the MBEA as well as weaker MMNm responses throughout the 6-month follow-up than the non-amusic patients or the amusic patients without AC damage. Furthermore, the amusic patients both with and without AC damage performed worse than the non-amusic patients on tests of working memory, attention, and cognitive flexibility. These findings suggest domain-general cognitive deficits to be the primary mechanism underlying amusia without AC damage whereas amusia with AC damage is associated with both auditory and cognitive deficits.

Effects of damage to auditory cortex on the discrimination of speech sounds by rats.

The intensity of a noise-induced startle response can be reduced by the presentation of an otherwise neutral stimulus immediately before the noise ("prepulse inhibition" or PPI). We used a form of PPI to study the effects of damage to auditory cortex on the discrimination of speech sounds by rats. Subjects underwent control surgery or treatment of the auditory cortex with the vasoconstrictor endothelin-1. This treatment caused damage concentrated in primary auditory cortex (A1). Both before and after lesions, subjects were tested on 5 tasks, most presenting a pair of human speech sounds (consonant-vowel syllables) so that the capacity for discrimination would be evident in the extent of PPI. Group comparisons failed to reveal any consistent lesion effect. At the same time, the analysis of individual differences in performance by multiple regression suggests that some of the temporal processing required to discriminate speech sounds is concentrated anteroventrally in the right A1. These results also confirm that PPI can be adapted to studies of the brain mechanisms involved in the processing of speech and other complex sounds.

Lesions of the auditory cortex impair azimuthal sound localization and its recalibration in ferrets.

The role of auditory cortex in sound localization and its recalibration by experience was explored by measuring the accuracy with which ferrets turned toward and approached the source of broadband sounds in the horizontal plane. In one group, large bilateral lesions were made of the middle ectosylvian gyrus, where the primary auditory cortical fields are located, and part of the anterior and/or posterior ectosylvian gyrus, which contain higher-level fields. In the second group, the lesions were intended to be confined to primary auditory cortex (A1). The ability of the animals to localize noise bursts of different duration and level was measured before and after the lesions were made. A1 lesions produced a modest disruption of approach-to-target responses to short-duration stimuli (<500 ms) on both sides of space, whereas head orienting accuracy was unaffected. More extensive lesions produced much greater auditory localization deficits, again primarily for shorter sounds. In these ferrets, the accuracy of both the approach-to-target behavior and the orienting responses was impaired, and they could do little more than correctly lateralize the stimuli. Although both groups of ferrets were still able to localize long-duration sounds accurately, they were, in contrast to ferrets with an intact auditory cortex, unable to relearn to localize these stimuli after altering the spatial cues available by reversibly plugging one ear. These results indicate that both primary and nonprimary cortical areas are necessary for normal sound localization, although only higher auditory areas seem to contribute to accurate head orienting behavior. They also show that the auditory cortex, and A1 in particular, plays an essential role in training-induced plasticity in adult ferrets, and that this is the case for both head orienting responses and approach-to-target behavior.

Fear conditioning to discontinuous auditory cues requires perirhinal cortical function.

Pretraining lesions of rat perirhinal (PR) cortex impair fear conditioning to ultrasonic vocalizations (USVs) but have no effect on conditioning to continuous tones. This study attempted to deconstruct USVs into simpler stimulus features that cause fear conditioning to be PR-dependent. Rats were conditioned to one of three cues: a multicall 19-kHz USV, a 19-kHz discontinuous tone, and a 19-kHz continuous tone. The discontinuous tone duplicated the on/off pattern of the individual calls in the USV, but it lacked the characteristic frequency modulations. Well-localized neurotoxic PR lesions impaired conditioning to the USV, the discontinuous tone, and the training context. However, PR lesions had no effect on conditioning to the continuous tone. The authors suggest that the lesion effects on fear conditioning to both cues and contexts reflect the essential role of PR in binding stimulus elements together into unitary representations.

Requirement of the auditory association cortex for discrimination of vowel-like sounds in rats.

We investigated the roles of the auditory cortex in discrimination learning of vowel-like sounds consisting of multiple formants. Rats were trained to discriminate between synthetic sounds with four formants. Bilateral electrolytic lesions including the primary auditory cortex and the dorsal auditory association cortex impaired multiformant discrimination, whereas they did not significantly affect discrimination between sounds with a single formant or between pure tones. Local lesions restricted to the dorsal/rostral auditory association cortex were sufficient to attenuate multiformant discrimination learning, and lesions restricted to the primary auditory cortex had no significant effects. These findings indicate that the dorsal/rostral auditory association cortex but not the primary auditory cortex is required for discrimination learning of vowel-like sounds with multiple formants in rats.

No indication of brain reorganization after unilateral ischemic lesions of the auditory cortex.

We used magnetoencephalography to study contralesional auditory reorganization in three men with chronic unilateral ischemic lesions of the auditory cortex. Although no response was found over the lesioned hemisphere, processing in the unaffected hemisphere was indistinguishable vs healthy controls. In contrast to sensorimotor and language systems, the auditory system seems to lack contralateral reorganization, presumably because patients are typically not aware of hearing deficits and thus do not perform training.

Comparison of estimates for volumes of brain ablations derived from structural MRI and classical histology.

Estimates of auditory cortex ablation sizes in a rodent model as derived from classical histology (volume reconstructions from Nissl-stained brain sections) and structural magnetic resonance imaging (MRI) (T1-weighted whole-brain scans from a 4.7 T animal scanner) were compared in the same specimens (Mongolian gerbils). Estimates of lesion volumes obtained with the two methods were very similar, robust, highly correlated and not significantly different from each other. Hence, the general usefulness of structural MRI for the determination of brain lesion size in small animal models is demonstrated. MRI therefore seems to be well suited to determine proper size and location of an experimental brain ablation prior to (potentially extensive) behavioral testing.

Natural antioxidant L-carnosine inhibits LPO intensification in structures of the auditory analyzer under conditions of chronic exposure to aminoglycoside antibiotics.

Intragastric administration of L-carnosine suspension to Wistar-Kyoto rats 3 days before and after 7-day course of intraperitoneal injections of ototoxic aminoglycoside antibiotic kanamycin compensated expenditures of tissue antioxidant systems and significantly eliminated kanamycin-induced intensification of MDA production in tissues of the membrane part of the cochlea and in the auditory cortex of the temporal lobe. L-NAME (competitive NO synthase inhibitor) also inhibited LPO, increased total antioxidant activity, and decreased ototoxicity of kanamycin, which confirms the contribution of NO into LPO intensification under conditions of aminoglycoside treatment. Inhibition of pathological intensification of LPO processes and increase in total antioxidant activity under conditions of induced acute aminoglycoside ototoxicity characterizes L-carnosine as a highly effective otoprotector.

Gap detection threshold in the rat before and after auditory cortex ablation.

Gap detection threshold (GDT) was measured in adult female pigmented rats (strain Long-Evans) by an operant conditioning technique with food reinforcement, before and after bilateral ablation of the auditory cortex. GDT was dependent on the frequency spectrum and intensity of the continuously present noise in which the gaps were embedded. The mean values of GDT for gaps embedded in white noise or low-frequency noise (upper cutoff frequency 3 kHz) at 70 dB sound pressure level (SPL) were 1.57+/-0.07 ms and 2.9+/-0.34 ms, respectively. Decreasing noise intensity from 80 dB SPL to 20 dB SPL produced a significant increase in GDT. The increase in GDT was relatively small in the range of 80-50 dB SPL for white noise and in the range of 80-60 dB for low-frequency noise. The minimal intensity level of the noise that enabled GDT measurement was 20 dB SPL for white noise and 30 dB SPL for low-frequency noise. Mean GDT values at these intensities were 10.6+/-3.9 ms and 31.3+/-4.2 ms, respectively. Bilateral ablation of the primary auditory cortex (complete destruction of the Te1 and partial destruction of the Te2 and Te3 areas) resulted in an increase in GDT values. The fifth day after surgery, the rats were able to detect gaps in the noise. The values of GDT observed at this time were 4.2+/-1.1 ms for white noise and 7.4+/-3.1 ms for low-frequency noise at 70 dB SPL. During the first month after cortical ablation, recovery of GDT was observed. However, 1 month after cortical ablation GDT still remained slightly higher than in controls (1.8+/-0.18 for white noise, 3.22+/-0.15 for low-frequency noise, P<0.05). A decrease in GDT values during the subsequent months was not observed.

Injury-induced reorganization in adult auditory cortex and its perceptual consequences.

Restricted cochlear lesions in adult animals result in a reorganization of auditory cortex such that the cortical region deprived of its normal input by the lesion is occupied by expanded representations of adjacent cochlear loci, and thus of the frequencies represented at those loci. Analogous injury-induced reorganization is seen in somatosensory, visual and motor cortices of adult animals after restricted peripheral lesions. The occurrence of such reorganization in a wide range of species (including simian primates), and across different sensory systems and forms of peripheral lesion, suggests that it would also occur in humans with similar lesions. Direct evidence in support of this suggestion is provided by a small body of functional imaging evidence in the somatosensory and auditory systems. Although such reorganization does not seem to have a compensatory function, such a profound change in the pattern of cortical activation produced by stimuli exciting peri-lesion parts of the receptor epithelium would be expected to have perceptual consequences. However, there is only limited psychophysical evidence for perceptual effects that might be attributable to injury-induced cortical reorganization, and very little direct evidence for the correlation between the perceptual phenomena and the occurrence of reorganization.