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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 refractory period T.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). A jump in the peak frequency in C reflects transitions of AM-tuning between low-pass and band-pass. Line types in D correspond to those in A.
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pcbi.1004997.g008: Effects of refractory period T.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). A jump in the peak frequency in C reflects transitions of AM-tuning between low-pass and band-pass. Line types in D correspond to those in A.

Mentions: In contrast to the coincidence threshold θ and window W, which affected the shape of the AM-tuning curve over the entire range, simulated effects of the refractory period T were limited to low modulation frequencies (Fig 8A). Variations of T affected the shape of the AM-tuning curve only below 300 Hz. For these low modulation frequencies, which are considerably lower than the half of the reciprocal of the coincidence window, two or more input coincidences could occur within the same modulation period, but because of the refractory period, not all coincidences led to output spikes. Hence a longer refractory period resulted in lower rates at low modulation frequencies without affecting the baseline (Fig 8A and 8B) and the corner frequency (Fig 8A and 8C). These observations suggest that a salient peak in the rate-MTF curve may be related to a refractory period > ~1.4 ms, and that monotonically decreasing rate-MTF (Fig 1A, red lines) may originate from a shorter refractory periods. As expected from the rate-MTF, the synch-MTF for fm > 300 Hz was not affected by the refractory period (Fig 8D).


Roles for Coincidence Detection in Coding Amplitude-Modulated Sounds.

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

Effects of refractory period T.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). A jump in the peak frequency in C reflects transitions of AM-tuning between low-pass and band-pass. 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.g008: Effects of refractory period T.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). A jump in the peak frequency in C reflects transitions of AM-tuning between low-pass and band-pass. Line types in D correspond to those in A.
Mentions: In contrast to the coincidence threshold θ and window W, which affected the shape of the AM-tuning curve over the entire range, simulated effects of the refractory period T were limited to low modulation frequencies (Fig 8A). Variations of T affected the shape of the AM-tuning curve only below 300 Hz. For these low modulation frequencies, which are considerably lower than the half of the reciprocal of the coincidence window, two or more input coincidences could occur within the same modulation period, but because of the refractory period, not all coincidences led to output spikes. Hence a longer refractory period resulted in lower rates at low modulation frequencies without affecting the baseline (Fig 8A and 8B) and the corner frequency (Fig 8A and 8C). These observations suggest that a salient peak in the rate-MTF curve may be related to a refractory period > ~1.4 ms, and that monotonically decreasing rate-MTF (Fig 1A, red lines) may originate from a shorter refractory periods. As expected from the rate-MTF, the synch-MTF for fm > 300 Hz was not affected by the refractory period (Fig 8D).

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