Binaural Hearing by the Mammalian Auditory Brainstem: Joint Coding of Interaural Level and Time Differences by the Lateral Superior Olive

Owrutsky, Zoe; Benichoux, Victor; Tollin, Daniel J.

doi:10.1007/978-3-030-57100-9_5

Cited by 5 publications

(4 citation statements)

References 87 publications

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“…Nevertheless, we expect that BICs (as well as binaural phase coding) are probably more vulnerable to a reduced temporal fidelity of input neurons than ILD coding. This hypothesis is a subject of future physiological studies in both onset (principal) and sustained (non-principal) neurons of young and aged animals examined with transient stimuli, such as AM sounds and clicks (for a recent review, see [ 73 ]).…”

Section: Discussionmentioning

confidence: 99%

Robustness of neuronal tuning to binaural sound localization cues against age-related loss of inhibitory synaptic inputs

2021

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Sound localization relies on minute differences in the timing and intensity of sound arriving at both ears. Neurons of the lateral superior olive (LSO) in the brainstem process these interaural disparities by precisely detecting excitatory and inhibitory synaptic inputs. Aging generally induces selective loss of inhibitory synaptic transmission along the entire auditory pathways, including the reduction of inhibitory afferents to LSO. Electrophysiological recordings in animals, however, reported only minor functional changes in aged LSO. The perplexing discrepancy between anatomical and physiological observations suggests a role for activity-dependent plasticity that would help neurons retain their binaural tuning function despite loss of inhibitory inputs. To explore this hypothesis, we use a computational model of LSO to investigate mechanisms underlying the observed functional robustness against age-related loss of inhibitory inputs. The LSO model is an integrate-and-fire type enhanced with a small amount of low-voltage activated potassium conductance and driven with (in)homogeneous Poissonian inputs. Without synaptic input loss, model spike rates varied smoothly with interaural time and level differences, replicating empirical tuning properties of LSO. By reducing the number of inhibitory afferents to mimic age-related loss of inhibition, overall spike rates increased, which negatively impacted binaural tuning performance, measured as modulation depth and neuronal discriminability. To simulate a recovery process compensating for the loss of inhibitory fibers, the strength of remaining inhibitory inputs was increased. By this modification, effects of inhibition loss on binaural tuning were considerably weakened, leading to an improvement of functional performance. These neuron-level observations were further confirmed by population modeling, in which binaural tuning properties of multiple LSO neurons were varied according to empirical measurements. These results demonstrate the plausibility that homeostatic plasticity could effectively counteract known age-dependent loss of inhibitory fibers in LSO and suggest that behavioral degradation of sound localization might originate from changes occurring more centrally.

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Section: Discussionmentioning

confidence: 99%

Robustness of neuronal tuning to binaural sound localization cues against age-related loss of inhibitory synaptic inputs

2021

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“…The bulk of the current evidence supports the hypothesis that the LSO, not the MSO, is the source of the BIC. Traditionally, the LSO has been thought to be the brainstem circuit responsible for encoding the ILD cue to location ( Tollin, 2003 ; Owrutsky et al, 2021 ). Recently, Benichoux et al (2018) showed that the function relating the amplitude of BIC DN1 to ITD was statistically indistinguishable across several rodent species, including in two species that do not have a binaurally functional MSO (mice and rats).…”

Section: Discussionmentioning

confidence: 99%

The Binaural Interaction Component in Rhesus Macaques (Macaca mulatta)

Peacock

Mackey

Benson

et al. 2021

eNeuro

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The binaural interaction component (BIC) is a sound-evoked electrophysiological signature of binaural processing in the auditory brainstem that has received attention as a potential biomarker for spatial hearing deficits. Yet the number of trials necessary to evoke the BIC, or its measurability, seems to vary across species: while it is easily measured in small rodents, it has proven to be highly variable and less reliably measured in humans. This has hindered its potential use as a diagnostic tool. Further measurements of the BIC across a wide range of species could help us better understand its origin and the possible reasons for the variation in its measurability. Statistical analysis on the function relating BIC DN1 amplitude and the interaural time difference has been performed in only a few small rodent species, thus it remains to be shown how the results apply to more taxonomically diverse mammals, and those with larger heads. To fill this gap, we measured BICs in rhesus macaque. We show the overall behavior of the BIC is the same as in smaller rodents, suggesting that the brainstem circuit responsible for the BIC is conserved across a wider range of mammals. We suggest that differences in measurability are likely because of differences in head size.

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“…It contains neurons in the ascending and the descending pathway, namely principal neurons (pLSOs) and lateral olivocochlear neurons (LOCs). pLSOs are involved in sound localization, whereas LOCs enable the central auditory system (CAS) to directly control the cochlear periphery (reviews: Friauf et al, 2019 ; Yin et al, 2019 ; Owrutsky et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Molecular and functional profiling of cell diversity and identity in the lateral superior olive, an auditory brainstem center with ascending and descending projections

Maraslioglu-Sperber,

Pizzi,

Fisch

et al. 2024

Front. Cell. Neurosci.

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The lateral superior olive (LSO), a prominent integration center in the auditory brainstem, contains a remarkably heterogeneous population of neurons. Ascending neurons, predominantly principal neurons (pLSOs), process interaural level differences for sound localization. Descending neurons (lateral olivocochlear neurons, LOCs) provide feedback into the cochlea and are thought to protect against acoustic overload. The molecular determinants of the neuronal diversity in the LSO are largely unknown. Here, we used patch-seq analysis in mice at postnatal days P10-12 to classify developing LSO neurons according to their functional and molecular profiles. Across the entire sample (n = 86 neurons), genes involved in ATP synthesis were particularly highly expressed, confirming the energy expenditure of auditory neurons. Two clusters were identified, pLSOs and LOCs. They were distinguished by 353 differentially expressed genes (DEGs), most of which were novel for the LSO. Electrophysiological analysis confirmed the transcriptomic clustering. We focused on genes affecting neuronal input–output properties and validated some of them by immunohistochemistry, electrophysiology, and pharmacology. These genes encode proteins such as osteopontin, Kv11.3, and Kvβ3 (pLSO-specific), calcitonin-gene-related peptide (LOC-specific), or Kv7.2 and Kv7.3 (no DEGs). We identified 12 “Super DEGs” and 12 genes showing “Cluster similarity.” Collectively, we provide fundamental and comprehensive insights into the molecular composition of individual ascending and descending neurons in the juvenile auditory brainstem and how this may relate to their specific functions, including developmental aspects.

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Binaural Hearing by the Mammalian Auditory Brainstem: Joint Coding of Interaural Level and Time Differences by the Lateral Superior Olive

Cited by 5 publications

References 87 publications

Robustness of neuronal tuning to binaural sound localization cues against age-related loss of inhibitory synaptic inputs

Robustness of neuronal tuning to binaural sound localization cues against age-related loss of inhibitory synaptic inputs

The Binaural Interaction Component in Rhesus Macaques (Macaca mulatta)

Molecular and functional profiling of cell diversity and identity in the lateral superior olive, an auditory brainstem center with ascending and descending projections

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