Directional Hearing by Linear Summation of Binaural Inputs at the Medial Superior Olive

Heijden, Marcel van der; Lorteije, Jeannette A. M.; Plauška, Andrius; Roberts, Michael; Golding, Nace L.; Borst, Jannie

doi:10.1016/j.neuron.2013.04.028

Cited by 90 publications

(86 citation statements)

References 65 publications

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“…It follows that a preceding of inhibition relative to excitation might be of crucial relevance for the computation of ITDs (5,26). Although the exact way the different MSO inputs are integrated to realize ITD resolution of about 30 μs on a single cell level is still highly controversial (22,(62)(63)(64), there is evidence for extraordinary temporal precision of the glycinergic MNTB input to the MSO including an experience-driven developmental selection of very few but strong inputs that show fast inhibitory postsynaptic currents (IPSCs)/inhibitory postsynaptic potentials (IPSPs). Our findings of morphological and physiological specializations in the inhibitory pathway strongly corroborate that not only fast, but precisely timed inhibition to the MSO is of central importance for the ITD processing mechanism.…”

Section: Discussionmentioning

confidence: 99%

Input timing for spatial processing is precisely tuned via constant synaptic delays and myelination patterns in the auditory brainstem

Stange-Marten¹,

Nabel²,

Sinclair³

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Precise timing of synaptic inputs is a fundamental principle of neural circuit processing. The temporal precision of postsynaptic input integration is known to vary with the computational requirements of a circuit, yet how the timing of action potentials is tuned presynaptically to match these processing demands is not well understood. In particular, action potential timing is shaped by the axonal conduction velocity and the duration of synaptic transmission delays within a pathway. However, it is not known to what extent these factors are adapted to the functional constraints of the respective circuit. Here, we report the finding of activity-invariant synaptic transmission delays as a functional adaptation for input timing adjustment in a brainstem sound localization circuit. We compared axonal and synaptic properties of the same pathway between two species with dissimilar timing requirements (gerbil and mouse): In gerbils (like humans), neuronal processing of sound source location requires exceptionally high input precision in the range of microseconds, but not in mice. Activityinvariant synaptic transmission and conduction delays were present exclusively in fast conducting axons of gerbils that also exhibited unusual structural adaptations in axon myelination for increased conduction velocity. In contrast, synaptic transmission delays in mice varied depending on activity levels, and axonal myelination and conduction velocity exhibited no adaptations. Thus, the specializations in gerbils and their absence in mice suggest an optimization of axonal and synaptic properties to the specific demands of sound localization. These findings significantly advance our understanding of structural and functional adaptations for circuit processing. myelination | synaptic transmission delay | sound localization | circuit processing | input timing T emporal integration of bioelectrical signals via chemical synapses is fundamental to neuronal computations. During circuit processing, neuronal information transfer via action potentials is controlled by exact differences in the occurrence between excitatory and inhibitory inputs (1-5). The arrival time of inputs within circuits in turn is largely shaped by the conduction delay of action potentials along the axons and during synaptic transmission. During ongoing activity, the transmission delays of chemical synapses generally increase in the range of hundreds of microseconds due to short-term adaptations (6-9). However, because temporal integration on postsynaptic neurons usually operates on time scales in the range of milliseconds or even longer (10, 11), sluggishness arising from synaptic mechanisms and axonal conductance is negligible for most of these computations. There are, however, some essential neuronal processing tasks that challenge the temporal precision of our nervous system. For instance, weakly electric fish detect miniature changes in the frequency of a constant electrical field. The neuronal circuits in these animals use electrical instead of chemical synapses in t...

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Section: Discussionmentioning

confidence: 99%

Input timing for spatial processing is precisely tuned via constant synaptic delays and myelination patterns in the auditory brainstem

Stange-Marten¹,

Nabel²,

Sinclair³

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Moreover, this may be different for threshold and suprathreshold functions. For directional hearing, merging of input from both sides occurs at the superior olivary nuclei [Grothe et al, 2010;van der Heijden et al, 2013]. Theoretical models, however, focus on threshold recognition at the brainstem level [Heil, 2014].…”

Section: Discussionmentioning

confidence: 99%

Binaural Auditory Outcomes in Patients with Postlingual Profound Unilateral Hearing Loss: 3 Years after Cochlear Implantation

et al. 2015

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The value of cochlear implants (CI) in patients with profound unilateral hearing loss (UHL) and tinnitus has recently been investigated. The authors previously demonstrated the feasibility of CI in a 12- month outcome study in a prospective UHL cohort. The aim of this study was to investigate the binaural auditory outcomes in this cohort 36 months after CI surgery. The 36-month outcome was evaluated in 22 CI users with postlingual UHL and severe tinnitus. Twelve subjects had contralateral normal hearing (single-sided deafness - SSD group) and 10 subjects had a contralateral, mild to moderate hearing loss and used a hearing aid (asymmetric hearing loss - AHL group). Speech perception in noise was assessed in two listening conditions: the CI_off and the CI_on condition. The binaural summation effect (S₀N₀), binaural squelch effect (S₀N_CI) and the combined head shadow effect (S_CIN₀) were investigated. Subjective benefit in daily life was assessed by means of the Speech, Spatial and Qualities of Hearing Scale (SSQ). At 36 months, a significant binaural summation effect was observed for the study cohort (2.00, SD 3.82 dB; p < 0.01) and for the AHL subgroup (3.34, SD 5.31 dB; p < 0.05). This binaural effect was not significant 12 months after CI surgery. A binaural squelch effect was significant for the AHL subgroup at 12 months (2.00, SD 4.38 dB; p < 0.05). A significant combined head shadow and squelch effect was also noted in the spatial configuration S_CIN₀ for the study cohort (4.00, SD 5.89 dB; p < 0.01) and for the AHL subgroup (5.67, SD 6.66 dB; p < 0.05). The SSQ data show that the perceived benefit in daily life after CI surgery remains stable up to 36 months at CI_on. CI can significantly improve speech perception in noise in patients with UHL. The positive effects of CI_on speech perception in noise increase over time up to 36 months after CI surgery. Improved subjective benefit in daily life was also shown to be sustained in these patients.

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“…The Cz-to-nape-of-the-neck channel was analyzed and is believed to reflect primarily inferior colliculus activity . Other nuclei in the auditory brainstem, such as the medial superior olive, also contribute to the FFR and are important to interaural time difference processing (van der Heijden et al 2013). Absolute electrode impedances were below 3 kΩ and interelectrode impedances were kept within 1 kΩ.…”

Section: Physiological Recordingsmentioning

confidence: 99%

“…Auditory brainstem processing related to BMLDs was suggested by theoretical models (Durlach 1963;Jeffress 1948), and has been confirmed in studies of animal electrophysiology in the medial superior olive (MSO) and inferior colliculus (IC) (Caird et al 1991;Du et al 2009b;Jiang et al 1997a;McAlpine et al 1996;Palmer et al 2000;van der Heijden et al 2013). In contrast, human literature has largely not found physiological correlates of BMLDs in brainstem auditory evoked potentials (BAEPs) (Fowler and Mikami 1996;Wilson and Krishnan 2005;Wong and Stapells 2004).…”

Section: Introductionmentioning

confidence: 97%

Neural Correlates of the Binaural Masking Level Difference in Human Frequency-Following Responses

Clinard

Hodgson

Scherer

2016

JARO

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The binaural masking level difference (BMLD) is an auditory phenomenon where binaural tone-in-noise detection is improved when the phase of either signal or noise is inverted in one of the ears (SN or SN, respectively), relative to detection when signal and noise are in identical phase at each ear (SN). Processing related to BMLDs and interaural time differences has been confirmed in the auditory brainstem of non-human mammals; in the human auditory brainstem, phase-locked neural responses elicited by BMLD stimuli have not been systematically examined across signal-to-noise ratio. Behavioral and physiological testing was performed in three binaural stimulus conditions: SN, SN, and SN. BMLDs at 500 Hz were obtained from 14 young, normal-hearing adults (ages 21-26). Physiological BMLDs used the frequency-following response (FFR), a scalp-recorded auditory evoked potential dependent on sustained phase-locked neural activity; FFR tone-in-noise detection thresholds were used to calculate physiological BMLDs. FFR BMLDs were significantly smaller (poorer) than behavioral BMLDs, and FFR BMLDs did not reflect a physiological release from masking, on average. Raw FFR amplitude showed substantial reductions in the SN condition relative to SN and SN conditions, consistent with negative effects of phase summation from left and right ear FFRs. FFR amplitude differences between stimulus conditions (e.g., SN amplitude-SN amplitude) were significantly predictive of behavioral SN BMLDs; individuals with larger amplitude differences had larger (better) behavioral B MLDs and individuals with smaller amplitude differences had smaller (poorer) behavioral B MLDs. These data indicate a role for sustained phase-locked neural activity in BMLDs of humans and are the first to show predictive relationships between behavioral BMLDs and human brainstem responses.

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Directional Hearing by Linear Summation of Binaural Inputs at the Medial Superior Olive

Cited by 90 publications

References 65 publications

Input timing for spatial processing is precisely tuned via constant synaptic delays and myelination patterns in the auditory brainstem

Input timing for spatial processing is precisely tuned via constant synaptic delays and myelination patterns in the auditory brainstem

Binaural Auditory Outcomes in Patients with Postlingual Profound Unilateral Hearing Loss: 3 Years after Cochlear Implantation

Neural Correlates of the Binaural Masking Level Difference in Human Frequency-Following Responses

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