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Auditory science tutorial. III: The role of the ascending pathways.

This paper attempts a thumbnail sketch of what is currently known about processing in the early parts of the auditory pathway. The paper briefly reviews the morphology and physiology of the auditory nuclei up to the inferior colliculi of the midbrain and discusses their function in processing sound information. Particular attention is paid to the role of these nuclei in sound localization and in analysing complex signals such as speech. One aim of the tutorial is to dispel any ideas that the peripheral auditory pathways are mere relays to the thalamus and cortex and to emphasize their fundamentally important role in auditory processing. The review is not comprehensive (indeed it can only touch upon some aspects of auditory processing) but key references are provided for those with more than just a passing interest.

Animals↗

Neural coding of relational invariance in speech: human language analogs to the barn owl.

The ability to form perceptual equivalence classes from variable input stimuli is common in both animals and humans. Neural circuitry that can disambiguate ambiguous stimuli to arrive at perceptual constancy has been documented in the barn owl's inferior colliculus where sound-source azimuth is signaled by interaural phase differences spanning the frequency spectrum of the sound wave. Extrapolating from the sound-localization system of the barn owl to human speech, 2 hypothetical models are offered to conceptualize the neural realization of relative invariance in (a) categorization of stop consonants/b, d, g/ across varying vowel contexts and (b) vowel identity across speakers. 2 computational algorithms employing real speech data were used to establish acoustic commonalities to form neural mappings representing phonemic equivalence classes in the form of functional arrays similar to those seen in the barn owl.

Adult↗

Interaural phase coding in auditory midbrain: influence of dynamic stimulus features.

A laterally located sound source stimulates the two ears at slightly different times, generating interaural phase disparities (IPDs) that are used for sound localization. Under natural conditions, such interaural cues are likely to be constantly changing, or dynamic. In the inferior colliculus of gerbils and cats, the nonlinearities in the coding of dynamic interaural phase cues are demonstrated. Responses to ecologically realistic phase cues are more reflective of the change of IPD than of the absolute IPDs over which that change occurs. This observation is inconsistent with the established view that directional information is coded in terms of absolute IPD.

Acoustic Stimulation↗

Frequency-following response: effects of interaural time and intensity differences.

This research investigated whether brainstem neural mechanisms that mediate lateralization of sounds can be extracted from the frequency-following response (FFR). Monaural and binaural FFRs were obtained from normal-hearing subjects to low-frequency (500 Hz) linearly gated tone bursts (4-4-4 msec) at 40, 50, and 60 dB SL and four interaural time differences (ITDs) (0, 333, 500, and 667 microsec). FFRs were also recorded to ITDs and intensity presented in concert and in opposition (lateralization stimuli). The results show that overall intensity and interaural time differentially affect the FFR. The FFRs evoked by ITDs and intensity (in concert and in opposition) are strikingly different. The normalized amplitudes of the binaural interaction component (BIC) are minimally altered by ITDs and intensity. The study presents strong evidence that ITDs of 0, 333, 500, and 667 microsec and lateralization stimuli, easily discriminated perceptually, evoke clearly distinguishable FFR waveforms. These ITDs provide the cues that mammals use to localize sound in a freefield. The BIC is essentially unaffected by overall intensity, ITDs, and lateralization stimuli. Based on the findings of this study, the FFR has the potential to become a tool for identification of normal and abnormal binaural processing at lower brainstem levels.

Adult↗

Interaural phase-sensitive units in the inferior colliculus of the unanesthetized rabbit: effects of changing frequency.

We studied the interaural phase sensitivity of 85 units in the inferior colliculus (IC) of the unanesthetized rabbit. We assessed this sensitivity at several frequencies within each unit's responsive range. The interaural phase disparity was varied by delivering tones that differed by 1 Hz to the two ears, resulting in a 1-Hz binaural beat. We analyzed each unit's response to different frequencies by calculating four measures: characteristic delay (CD), characteristic phase (CP), composite peak delay, and mean peak delay. We estimated the CD and CP from the slope and phase intercept, respectively, of the regression line fitted to a plot of the mean interaural phase against stimulating frequency. The composite peak delay was estimated from the peak of a composite delay curve. This was generated by replotting the response to changes in interaural phase, as a function of the equivalent interaural delay and averaging the resultant interaural delay curves. The composite delay curve reflects the unit's average response to interaural delays across frequencies. Last, we calculated a mean peak delay, derived by converting the mean interaural phase of the response at each frequency to an equivalent delay and then averaging these delays. Interaural phase sensitivity was observed to frequencies as high as 2,150 Hz. However, the majority of units showed such sensitivity below 1,500 Hz. For most units, the interaural delay curves measured at several frequencies coincided near the peak discharge. This result is consistent with a neural model, where excitatory inputs from each ear converge upon a binaural cell, evoking maximum discharge only when the two inputs arrive simultaneously. As a first approximation, our data fit this model, indicating that IC neurons can act like coincidence detectors or cross-correlators. The distributions of CD, composite peak delay, and mean peak delay showed that most units preferred ipsilateral stimulus delays, which in the natural situation corresponds to sounds emanating from the contralateral field. Moreover, most units preferred delays that were within the estimated physiological range of the rabbit. These results support the viewpoint that neurons in the IC participate in sound localization. The distributions of CP and CD differ substantially from those found in the IC of the anesthetized cat. These differences may reflect species differences, the effects of anesthesia, or a difference in the population of units sampled. For each unit, we assessed the linearity of the plot of mean interaural phase against frequency of stimulation using a chi 2 method. For most units the plots were significantly nonlinear.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

New neural circuits for robot phonotaxis.

W. Grey Walter built robotic systems to improve understanding of biological systems. In that tradition, this paper reports ongoing work on a robot model of cricket sound localization. The main advances are the inclusion of a much larger range of neuroethological detail, and the investigation of multimodal influences on the behaviour. The former allows exploration of the functionality of identified neurons in the insect, including the possible roles of multiple sensory fibres, mutually inhibitory connections, and brain neurons with pattern-filtering properties. The latter focuses on the inclusion of an optomotor stabilization response, and how this might improve tracking, particularly under conditions of random disturbance.

Animal Communication↗

Comparison of the bone anchored hearing aid implantable hearing device with contralateral routing of offside signal amplification in the rehabilitation of unilateral deafness.

OBJECTIVE: Monaural hearing imposes constraints under many listening conditions. The authors compared the effects of a semi-implantable bone conductor, the Entific bone anchored hearing aid, with conventional contralateral routing of offside signal amplification to assess rehabilitative benefit in adults with unilateral deafness. DESIGN: Prospective trials of subjects with unilateral deafness using benefit surveys, source identification testing, and hearing in noise testing. SETTING: Tertiary referral center, outpatient surgical and audiologic services. PATIENTS: Adults with unilateral deafness (pure tone average >90 dB, SD <20%) after acoustic neuroma excision (n = 7), meningitis (n = 1), sudden sensorineural hearing loss (n = 1), and sudden sensorineural hearing loss with chronic suppurative otitis media (n = 1). Entry criteria included normal hearing in the contralateral ear (pure tone average <25 dB, SD >80%). INTERVENTION: Subjects were fitted with contralateral routing of offside signal amplification devices for 1 month and tested with contralateral routing of offside signal before mastoid implantation of the deaf ear, fitting, and testing for bone anchored hearing aid. OUTCOME MEASURES: Subjects' assessment of experience with their devices and patterns of use, 2) source azimuth identification in noise test, and 3) speech discrimination in quiet and in noise under conditions of noise-front, noise-to-normal-ear, and noise-to-deaf-ear. RESULTS: There was consistent satisfaction with bone anchored hearing aid implantation and amplification, and poor acceptance of contralateral routing of offside signal amplification. Sound localization was poor at baseline and with both bone anchored hearing aid and contralateral routing of offside signal. Relative to baseline, contralateral routing of offside signal and bone anchored hearing aid produced significantly better speech recognition in noise under most conditions. The bone anchored hearing aid enabled significantly better speech recognition than contralateral routing of offside signal in quiet and in a composite of noise conditions. The advantages may relate to averting the interference of speech signals delivered to the better ear, as occurs with conventional contralateral routing of offside signal amplification. CONCLUSIONS: Preliminary data in subjects with normal monaural hearing indicate that vibromechanical stimulation with the bone anchored hearing aid overcomes some of the negative head shadow effects in unilateral deafness. The bone anchored hearing aid system, when placed on the side of a deaf ear, yields greater benefit in subjects with normal monaural hearing than does contralateral routing of offside signal amplification. It seems that this rehabilitative approach can expand the sound field of monaural listeners in further enhancing speech understanding. Observations suggest that further understanding of bone conduction as implemented in transcranial stimulation will guide further options for patients with monaural hearing. Longer follow-up will help to determine whether communicative skill improvements with the bone anchored hearing aid outweigh the disadvantages of implantation surgery, costs, and device maintenance.

Adult↗

Elimination and strengthening of glycinergic/GABAergic connections during tonotopic map formation.

Synapse elimination and strengthening are central mechanisms for the developmental organization of excitatory neuronal networks. Little is known, however, about whether these processes are also involved in establishing precise inhibitory circuits. We examined the development of functional connectivity before hearing onset in rats in the tonotopically organized, glycinergic pathway from the medial nucleus of the trapezoid body (MNTB) to the lateral superior olive (LSO), which is part of the mammalian sound localization system. We found that LSO neurons became functionally disconnected from approximately 75% of their initial inputs, resulting in a two-fold sharpening of functional topography. This was accompanied by a 12-fold increase in the synaptic conductance generated by maintained individual inputs. Functional elimination of MNTB-LSO synapses was restricted to the period when these glycinergic/GABAergic synapses are excitatory. These results provide new insights into the mechanisms by which precisely organized inhibitory circuits are established during development.

Aging↗

Restoration of acoustic orienting into a cortically deaf hemifield by reversible deactivation of the contralesional superior colliculus: the acoustic "Sprague Effect".

Removal of all contiguous visual cortical areas of one hemisphere results in a contralateral hemianopia. Subsequent deactivation of the contralesional superior colliculus (SC) nullifies the effects of the visual cortex ablation and restores visual orienting responses into the cortically blind hemifield. This deficit nullification has become known as the "Sprague Effect." Similarly, in the auditory system, unilateral ablation of auditory cortex results in severe sound localization deficits, as assessed by acoustic orienting, to stimuli in the contralateral hemifield. The purpose of this study was to examine whether auditory orienting responses can be restored into the impaired hemifield during deactivation of the contralesional SC. Three mature cats were trained to orient toward and approach an acoustic stimulus (broadband, white noise burst) that was presented centrally, or at one of 12 peripheral loci, spaced at 15 degrees intervals. After training, a cryoloop was chronically implanted over the dorsal surface of the right SC. During cooling of the cooling loop to temperatures sufficient to deactivate the superficial and intermediate layers (SZ, SGS, SO, SGI), auditory orienting responses were eliminated into the left (contracooled) hemifield while leaving acoustic orienting into the right (ipsicooled) hemifield unimpaired. This deficit was temperature-dependently graded from periphery to center. After the effectiveness of the SC cooling loop was verified, auditory cortex of the middle and posterior ectosylvian and anterior and posterior sylvian gyri was removed from the left hemisphere. As expected, the auditory cortex ablation resulted in a profound deficit in orienting to acoustic stimuli presented at any position in the right (contralesional) hemifield, while leaving acoustic orienting into the left (ipsilesional) hemifield unimpaired. The ablations of auditory cortex did not have any impact on a visual detection and orienting task. The additional deactivation of the contralesional SC to temperatures sufficient to cool the superficial and intermediate layers nullified the deficit caused by the auditory cortex ablation and acoustic orienting responses were restored into the right hemifield. This restoration was temperature-dependently graded from center to periphery. The deactivations were localized and confirmed with reduced uptake of radiolabeled 2-deoxyglucose. Therefore deactivation of the right superior colliculus after the ablation of the left auditory cortex yields a fundamentally different result from that identified during deactivation of the right superior colliculus before the removal of left auditory cortex in the same animal. Thus the "Sprague Effect" is not unique to a particular sensory system and deactivation of the contralesional SC can restore either visual or acoustic orienting responses into an impaired hemifield after cortical damage.

Acoustic Stimulation↗

Axonal delay lines for time measurement in the owl's brainstem.

Interaural time difference is an important cue for sound localization. In the barn owl (Tyto alba) neuronal sensitivity to this disparity originates in the brainstem nucleus laminaris. Afferents from the ipsilateral and contralateral magnocellular cochlear nuclei enter the nucleus laminaris through its dorsal and ventral surfaces, respectively, and interdigitate in the nucleus. Intracellular recordings from these afferents show orderly changes in conduction delay with depth in the nucleus. These changes are comparable to the range of interaural time differences available to the owl. Thus, these afferent axons act as delay lines and provide anatomical and physiological bases for a neuronal map of interaural time differences in the nucleus laminaris.

Animals↗

Brain functional reorganization in early blind humans revealed by auditory event-related potentials.

Visually challenged individuals often compensate for their handicap by developing supra-normal abilities in their remaining sensory systems. Here, we examined the scalp distribution of components N1 and P3 of auditory evoked potentials during a sound localization task in four totally blind subjects who had previously shown better performance than sighted subjects. Both N1 and P3 waves peaked at their usual positions while blind and sighted individuals performed the task. However, in blind subjects these two components were also found to be robust over occipital regions while in sighted individuals this pattern was not seen. We conclude that deafferented posterior visual areas in blind individuals are recruited to carry out auditory functions, enabling these individuals to compensate for their lack of vision.

Acoustic Stimulation↗

Auditory and visual space maps in the cholinergic nucleus isthmi pars parvocellularis of the barn owl.

The nucleus isthmi pars parvocellularis (Ipc) is a midbrain cholinergic nucleus that shares reciprocal, topographic connections with the optic tectum (OT). Ipc neurons project to spatially restricted columns in the OT, contacting essentially all OT layers in a given column. Previous research characterizes the Ipc as a visual processor. We found that, in the barn owl, the Ipc responds to auditory as well as to visual stimuli. Auditory responses were tuned broadly for frequency, but sharply for spatial cues. We measured the tuning of Ipc units to binaural sound localization cues, including interaural timing differences (ITDs) and interaural level differences (ILDs). Units in the Ipc were tuned to specific values of both ITD and ILD and were organized systematically according to their ITD and ILD tuning, forming a map of space. The auditory space map aligned with the visual space map in the Ipc. These results demonstrate that the Ipc encodes the spatial location of objects, independent of stimulus modality. These findings, combined with the precise pattern of projections from the Ipc to the OT, suggest that the role of the Ipc is to regulate the sensitivity of OT neurons in a space-specific manner.

Acoustic Stimulation↗

Endbulb synapses in the anteroventral cochlear nucleus express a specific subset of AMPA-type glutamate receptor subunits.

The anteroventral cochlear nucleus (AVCN) acts as the first relay center in the conduction of auditory information from the ear to the brain, and it probably performs a crucial role in sound localization. Auditory nerve input to the principal neurons of the AVCN, the spherical bushy cells, appears to be mediated by an excitatory amino acid such as glutamate, which acts at a specialized, large synaptic ending called an endbulb of Held. Presumably, endbulb synapses contain some specific combination of glutamate receptors to facilitate rapid neurotransmission of auditory signals. AMPA glutamate receptor composition at the endbulb synapses was examined with both light and electron microscope immunocytochemistry. Electron microscope localization of AMPA receptors was examined with two techniques, preembedding immunoperoxidase and postembedding immunogold, which provide maximum sensitivity and greatest accuracy, respectively. Dense and frequent labeling was seen with the AMPA receptor subunit antibodies GluR2/3 and GluR4, which were colocalized at the endbulb synapses. In contrast, immunolabeling with antibody to GluR2 was low. These data indicate that the major glutamate receptor at this synapse is an AMPA receptor made up mainly of GluR3 and GluR4 subunits. Receptors composed of these subunits display properties, such as calcium permeability and rapid desensitization, that facilitate their specialized functions in auditory information processing.

Animals↗

Influence of the facial ruff on the sound-receiving characteristics of the barn owl's ears.

The barn owl, a nocturnal predator, derives its German name ("Schleiereule", direct English translation "veil owl") from the conspicuous ruff that covers the ear openings and gives the head a face-like appearance. The ruff is a specialization for the perception of sound. The densely-ramified reflector feathers forming the border of the ruff direct sound to the ear-openings. We studied the influence of the ruff on the behaviorally relevant sound-localization parameters interaural time difference (ITD) and interaural level difference (ILD). The directionality of the ear was much greater when the ruff was intact than when the reflector feathers were removed. With ruff intact, the distribution of ILDs was oblique and the maximum ITD occurred around 110 degrees of azimuth. When all head feathers were removed, the steepest ILD gradient was much closer to the horizontal axis and ITD was maximal at 90 degrees . Many effects were frequency specific. Thus, the ruff reflects some properties of the human pinna. However, by shifting the point where ITD becomes maximal beyond 90 degrees , the ruff also introduces a break of the front-back symmetry of ITD.

Acoustic Stimulation↗

Usage of CROS and IROS hearing aids by patients with bilateral high-frequency hearing loss.

Responses to a hearing aid usage questionnaire were received from 128 patients with high-frequency sensorineural hearing loss fitted monaurally with contralateral routing of signals (CROS) or ipsilateral routing of signals (IROS) hearing aids. Functional benefits were demonstrated by wearing the instruments 8 to 9 hr/day, use of the aids about 60% of the time in communicative situations, subjective benefit judgements of 5 to 9 on a 10-point scale, improved subjective sound localization, and improved clarity of speech with the hearing aids. Although CROS and IROS fittings could not be separated on the basis of these factors, considerably more complaints were reported by the CROS wearers, and many of these related to auditory factors. Both CROS and IROS fittings appear to be effective approaches to the patient with high-frequency hearing loss. However in light of the fewer complaints by the IROS group, and the fact that a large proportion of the CROS complaints related to the amplified signal, IROS appears to be the preferable of the two. The exception involves cases requiring high gain so that CROS might be employed to reduce acoustic feedback.

Consumer Behavior↗

Precedence effect and speech understanding in elderly listeners.

It has been reported that many elderly persons exhibit problems in identifying the location of fused auditory images in a test of the precedence effect in sound localization. The precedence effect involves the neural integration of multiple competing binaural temporal cues, and may reflect subtle age-related neural timing or integration problems. This study investigated whether elderly persons who have difficulty with this test also exhibit problems with speech understanding. The speech measures involved a comparison of performance-intensity functions for phonetically balanced (PB) words and for synthetic sentences presented with ipsilateral speech competition (SSI-ICM). The performance of the elderly subjects on the precedence effect test was significantly correlated with the SSI-max scores but not with PB-max. These findings suggest that age-related difficulties in speech understanding may reflect, at least in part, breakdowns in auditory temporal acuity or resolution.

Acoustic Stimulation↗

Developmental changes underlying the formation of the specialized time coding circuits in barn owls (Tyto alba).

Barn owls are capable of great accuracy in detecting the interaural time differences (ITDs) that underlie azimuthal sound localization. They compute ITDs in a circuit in nucleus laminaris (NL) that is reorganized with respect to birds like the chicken. The events that lead to the reorganization of the barn owl NL take place during embryonic development, shortly after the cochlear and laminaris nuclei have differentiated morphologically. At first the developing owl's auditory brainstem exhibits morphology reminiscent of that of the developing chicken. Later, the two systems diverge, and the owl's brainstem auditory nuclei undergo a secondary morphogenetic phase during which NL dendrites retract, the laminar organization is lost, and synapses are redistributed. These events lead to the restructuring of the ITD coding circuit and the consequent reorganization of the hindbrain map of ITDs and azimuthal space.

Animals↗

Commissural connections mediate inhibition for the computation of interaural level difference in the barn owl.

In the barn owl (Tyto alba), the posterior nucleus of the ventral lateral lemniscus (VLVp) is the first site of binaural convergence in the pathway that processes interaural level difference (ILD), an important sound-localization cue. The neurons of VLVp are sensitive to ILD because of an excitatory input from the contralateral ear and an inhibitory input from the ipsilateral ear. A previously described projection from the contralateral cochlear nucleus, can account for the excitation. The present study addresses the source of the inhibitory input. We demonstrate with standard axonal transport methods that the left and right VLVps are interconnected via fibers of the commissure of Probst. We further show that the anesthetization of one VLVp renders ineffective the inhibition that is normally evoked by stimulation of the ipsilateral ear. Thus, one cochlear nucleus (driven by the ipsilateral ear) appears to provide inhibition to the ipsilateral VLVp by exciting commissurally-projecting inhibitory neurons in the contralateral VLVp.

Animals↗