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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.


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Effects of coincidence threshold θ.A: AM-tuning curves (rate-MTFs). B: Peak and baseline spike rates. C: Peak and corner frequencies of the rate-MTFs. D: Modulation gains (synch-MTFs). Line types in D correspond to those in A.
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pcbi.1004997.g004: Effects of coincidence threshold θ.A: AM-tuning curves (rate-MTFs). B: Peak and baseline spike rates. C: Peak and corner frequencies of the rate-MTFs. D: Modulation gains (synch-MTFs). Line types in D correspond to those in A.

Mentions: Fig 4 summarizes the effects of the coincidence threshold θ on monaural AM-tuning. The choice of coincidence threshold θ greatly affected the response rates of the modeled LSO neuron to AM sounds (Fig 4A). Decreased thresholds led to higher baseline rates as well as to higher peak rates (Fig 4A and 4B). With lower thresholds, peak and half-peak frequencies shifted to higher modulation frequencies (Fig 4A and 4C). For a high threshold (θ = 10 in Fig 4A), the AM-tuning curve was monotonic, with a peak frequency being close to zero Hz. Thus rate-MTF curves of LSO neurons with low thresholds tended to be shifted both to higher spike rates and to higher modulation frequencies. These observations suggest that LSO neurons with low rate-MTF (Fig 1A, orange lines) may have high coincidence thresholds, whereas those with high average spike rates over the entire frequency range (Fig 1A, green lines) may have low thresholds.


Roles for Coincidence Detection in Coding Amplitude-Modulated Sounds.

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

Effects of coincidence threshold θ.A: AM-tuning curves (rate-MTFs). B: Peak and baseline spike rates. C: Peak and corner frequencies of the rate-MTFs. D: Modulation gains (synch-MTFs). Line types in D correspond to those in A.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4920552&req=5

pcbi.1004997.g004: Effects of coincidence threshold θ.A: AM-tuning curves (rate-MTFs). B: Peak and baseline spike rates. C: Peak and corner frequencies of the rate-MTFs. D: Modulation gains (synch-MTFs). Line types in D correspond to those in A.
Mentions: Fig 4 summarizes the effects of the coincidence threshold θ on monaural AM-tuning. The choice of coincidence threshold θ greatly affected the response rates of the modeled LSO neuron to AM sounds (Fig 4A). Decreased thresholds led to higher baseline rates as well as to higher peak rates (Fig 4A and 4B). With lower thresholds, peak and half-peak frequencies shifted to higher modulation frequencies (Fig 4A and 4C). For a high threshold (θ = 10 in Fig 4A), the AM-tuning curve was monotonic, with a peak frequency being close to zero Hz. Thus rate-MTF curves of LSO neurons with low thresholds tended to be shifted both to higher spike rates and to higher modulation frequencies. These observations suggest that LSO neurons with low rate-MTF (Fig 1A, orange lines) may have high coincidence thresholds, whereas those with high average spike rates over the entire frequency range (Fig 1A, green lines) may have low thresholds.

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