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

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 sele...

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Autores principales:	Go Ashida, Daniel J Tollin, Jutta Kretzberg
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/b0425b8dd1b94634a8f90d12cb856039
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spelling	oai:doaj.org-article:b0425b8dd1b94634a8f90d12cb8560392021-12-02T19:57:33ZRobustness of neuronal tuning to binaural sound localization cues against age-related loss of inhibitory synaptic inputs.1553-734X1553-735810.1371/journal.pcbi.1009130https://doaj.org/article/b0425b8dd1b94634a8f90d12cb8560392021-07-01T00:00:00Zhttps://doi.org/10.1371/journal.pcbi.1009130https://doaj.org/toc/1553-734Xhttps://doaj.org/toc/1553-7358Sound 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.Go AshidaDaniel J TollinJutta KretzbergPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Computational Biology, Vol 17, Iss 7, p e1009130 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Go Ashida Daniel J Tollin Jutta Kretzberg Robustness of neuronal tuning to binaural sound localization cues against age-related loss of inhibitory synaptic inputs.
description	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.
format	article
author	Go Ashida Daniel J Tollin Jutta Kretzberg
author_facet	Go Ashida Daniel J Tollin Jutta Kretzberg
author_sort	Go Ashida
title	Robustness of neuronal tuning to binaural sound localization cues against age-related loss of inhibitory synaptic inputs.
title_short	Robustness of neuronal tuning to binaural sound localization cues against age-related loss of inhibitory synaptic inputs.
title_full	Robustness of neuronal tuning to binaural sound localization cues against age-related loss of inhibitory synaptic inputs.
title_fullStr	Robustness of neuronal tuning to binaural sound localization cues against age-related loss of inhibitory synaptic inputs.
title_full_unstemmed	Robustness of neuronal tuning to binaural sound localization cues against age-related loss of inhibitory synaptic inputs.
title_sort	robustness of neuronal tuning to binaural sound localization cues against age-related loss of inhibitory synaptic inputs.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/b0425b8dd1b94634a8f90d12cb856039
work_keys_str_mv	AT goashida robustnessofneuronaltuningtobinauralsoundlocalizationcuesagainstagerelatedlossofinhibitorysynapticinputs AT danieljtollin robustnessofneuronaltuningtobinauralsoundlocalizationcuesagainstagerelatedlossofinhibitorysynapticinputs AT juttakretzberg robustnessofneuronaltuningtobinauralsoundlocalizationcuesagainstagerelatedlossofinhibitorysynapticinputs
_version_	1718375795768950784

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

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