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Roles for Coincidence Detection in Coding Amplitude-Modulated Sounds.

Ashida G, Kretzberg J, Tollin DJ - PLoS Comput. Biol. (2016)

Bottom Line: Previous physiological recordings in vivo found considerable variations in monaural AM-tuning across neurons.Unlike monaural AM coding, temporal factors, such as the coincidence window and the effective duration of inhibition, played a major role in determining the trough positions of simulated binaural phase-response curves.These modeling results suggest that coincidence detection of excitatory and inhibitory synaptic inputs is essential for LSO neurons to encode both monaural and binaural AM sounds.

View Article: PubMed Central - PubMed

Affiliation: Cluster of Excellence "Hearing4all", Department for Neuroscience, Faculty 6, University of Oldenburg, Oldenburg, Germany.

ABSTRACT
Many sensory neurons encode temporal information by detecting coincident arrivals of synaptic inputs. In the mammalian auditory brainstem, binaural neurons of the medial superior olive (MSO) are known to act as coincidence detectors, whereas in the lateral superior olive (LSO) roles of coincidence detection have remained unclear. LSO neurons receive excitatory and inhibitory inputs driven by ipsilateral and contralateral acoustic stimuli, respectively, and vary their output spike rates according to interaural level differences. In addition, LSO neurons are also sensitive to binaural phase differences of low-frequency tones and envelopes of amplitude-modulated (AM) sounds. Previous physiological recordings in vivo found considerable variations in monaural AM-tuning across neurons. To investigate the underlying mechanisms of the observed temporal tuning properties of LSO and their sources of variability, we used a simple coincidence counting model and examined how specific parameters of coincidence detection affect monaural and binaural AM coding. Spike rates and phase-locking of evoked excitatory and spontaneous inhibitory inputs had only minor effects on LSO output to monaural AM inputs. In contrast, the coincidence threshold of the model neuron affected both the overall spike rates and the half-peak positions of the AM-tuning curve, whereas the width of the coincidence window merely influenced the output spike rates. The duration of the refractory period affected only the low-frequency portion of the monaural AM-tuning curve. Unlike monaural AM coding, temporal factors, such as the coincidence window and the effective duration of inhibition, played a major role in determining the trough positions of simulated binaural phase-response curves. In addition, empirically-observed level-dependence of binaural phase-coding was reproduced in the framework of our minimalistic coincidence counting model. These modeling results suggest that coincidence detection of excitatory and inhibitory synaptic inputs is essential for LSO neurons to encode both monaural and binaural AM sounds.

No MeSH data available.


Related in: MedlinePlus

Effects of spontaneous inhibitory inputs.A: AM-tuning curves (rate-MTFs). B: Modulation gains (synch-MTFs). Curves for θ = 8 (default threshold: thick lines) and 7 (reduced threshold: thin line) are shown for comparison. Spontaneous rates λinh of inhibitory inputs were: 0 (no inhibition), 30 (default) and 60 (doubled inhibition).
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pcbi.1004997.g009: Effects of spontaneous inhibitory inputs.A: AM-tuning curves (rate-MTFs). B: Modulation gains (synch-MTFs). Curves for θ = 8 (default threshold: thick lines) and 7 (reduced threshold: thin line) are shown for comparison. Spontaneous rates λinh of inhibitory inputs were: 0 (no inhibition), 30 (default) and 60 (doubled inhibition).

Mentions: MNTB neurons that send inhibitory projections to LSO are spontaneously active [23,50]. Effects of spontaneous inhibition on the AM-tuning curve, however, were found to be limited (Fig 9A). Removal of inhibition only resulted in a slight increase in the rate of response to monaural stimulation. Simple calculations may explain these limited effects of inhibition. Assuming that an LSO neuron receives 8 inhibitory inputs with a spike rate of 30 spikes/sec and that each inhibitory input elevates the threshold by 2 with an effective time window of 1.6 ms, the time-averaged threshold increase can be estimated as: 8×30×1.6×10−3×2 = 0.768 inputs. Therefore the average effect of spontaneous inhibition is expected to be smaller than the effect of changing the threshold by one.


Roles for Coincidence Detection in Coding Amplitude-Modulated Sounds.

Ashida G, Kretzberg J, Tollin DJ - PLoS Comput. Biol. (2016)

Effects of spontaneous inhibitory inputs.A: AM-tuning curves (rate-MTFs). B: Modulation gains (synch-MTFs). Curves for θ = 8 (default threshold: thick lines) and 7 (reduced threshold: thin line) are shown for comparison. Spontaneous rates λinh of inhibitory inputs were: 0 (no inhibition), 30 (default) and 60 (doubled inhibition).
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4920552&req=5

pcbi.1004997.g009: Effects of spontaneous inhibitory inputs.A: AM-tuning curves (rate-MTFs). B: Modulation gains (synch-MTFs). Curves for θ = 8 (default threshold: thick lines) and 7 (reduced threshold: thin line) are shown for comparison. Spontaneous rates λinh of inhibitory inputs were: 0 (no inhibition), 30 (default) and 60 (doubled inhibition).
Mentions: MNTB neurons that send inhibitory projections to LSO are spontaneously active [23,50]. Effects of spontaneous inhibition on the AM-tuning curve, however, were found to be limited (Fig 9A). Removal of inhibition only resulted in a slight increase in the rate of response to monaural stimulation. Simple calculations may explain these limited effects of inhibition. Assuming that an LSO neuron receives 8 inhibitory inputs with a spike rate of 30 spikes/sec and that each inhibitory input elevates the threshold by 2 with an effective time window of 1.6 ms, the time-averaged threshold increase can be estimated as: 8×30×1.6×10−3×2 = 0.768 inputs. Therefore the average effect of spontaneous inhibition is expected to be smaller than the effect of changing the threshold by one.

Bottom Line: Previous physiological recordings in vivo found considerable variations in monaural AM-tuning across neurons.Unlike monaural AM coding, temporal factors, such as the coincidence window and the effective duration of inhibition, played a major role in determining the trough positions of simulated binaural phase-response curves.These modeling results suggest that coincidence detection of excitatory and inhibitory synaptic inputs is essential for LSO neurons to encode both monaural and binaural AM sounds.

View Article: PubMed Central - PubMed

Affiliation: Cluster of Excellence "Hearing4all", Department for Neuroscience, Faculty 6, University of Oldenburg, Oldenburg, Germany.

ABSTRACT
Many sensory neurons encode temporal information by detecting coincident arrivals of synaptic inputs. In the mammalian auditory brainstem, binaural neurons of the medial superior olive (MSO) are known to act as coincidence detectors, whereas in the lateral superior olive (LSO) roles of coincidence detection have remained unclear. LSO neurons receive excitatory and inhibitory inputs driven by ipsilateral and contralateral acoustic stimuli, respectively, and vary their output spike rates according to interaural level differences. In addition, LSO neurons are also sensitive to binaural phase differences of low-frequency tones and envelopes of amplitude-modulated (AM) sounds. Previous physiological recordings in vivo found considerable variations in monaural AM-tuning across neurons. To investigate the underlying mechanisms of the observed temporal tuning properties of LSO and their sources of variability, we used a simple coincidence counting model and examined how specific parameters of coincidence detection affect monaural and binaural AM coding. Spike rates and phase-locking of evoked excitatory and spontaneous inhibitory inputs had only minor effects on LSO output to monaural AM inputs. In contrast, the coincidence threshold of the model neuron affected both the overall spike rates and the half-peak positions of the AM-tuning curve, whereas the width of the coincidence window merely influenced the output spike rates. The duration of the refractory period affected only the low-frequency portion of the monaural AM-tuning curve. Unlike monaural AM coding, temporal factors, such as the coincidence window and the effective duration of inhibition, played a major role in determining the trough positions of simulated binaural phase-response curves. In addition, empirically-observed level-dependence of binaural phase-coding was reproduced in the framework of our minimalistic coincidence counting model. These modeling results suggest that coincidence detection of excitatory and inhibitory synaptic inputs is essential for LSO neurons to encode both monaural and binaural AM sounds.

No MeSH data available.


Related in: MedlinePlus