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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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Response of pure integrator model.A: Simulated monaural AM-tuning curves (rate-MTFs). B: Modulation gains (synch-MTFs). C: Binaural phase-tuning curves at different frequencies. The same input parameter set as for Fig 2D and 2E was used. The threshold was fixed to 8 inputs in C.
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pcbi.1004997.g014: Response of pure integrator model.A: Simulated monaural AM-tuning curves (rate-MTFs). B: Modulation gains (synch-MTFs). C: Binaural phase-tuning curves at different frequencies. The same input parameter set as for Fig 2D and 2E was used. The threshold was fixed to 8 inputs in C.

Mentions: Simulated rate-MTF curves of the pure integrator showed a broad tuning (Fig 14A), which resembles the all-pass property of input fibers (Fig 2A). The response rates were slightly reduced at low frequencies (< 300 Hz) where the refractory period plays a role. Simulated synch-MTFs of the pure integrator showed a high gain (> 3 dB) for only a narrow range of modulation frequencies (Fig 14B). For other frequencies, gains were generally lower than the coincidence counting model (Fig 4D) and physiological data [36]. Thus the responses of the pure integrator were largely inconsistent with empirical LSO responses to monaural AM sounds (Fig 1A and [36]).


Roles for Coincidence Detection in Coding Amplitude-Modulated Sounds.

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

Response of pure integrator model.A: Simulated monaural AM-tuning curves (rate-MTFs). B: Modulation gains (synch-MTFs). C: Binaural phase-tuning curves at different frequencies. The same input parameter set as for Fig 2D and 2E was used. The threshold was fixed to 8 inputs in C.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4920552&req=5

pcbi.1004997.g014: Response of pure integrator model.A: Simulated monaural AM-tuning curves (rate-MTFs). B: Modulation gains (synch-MTFs). C: Binaural phase-tuning curves at different frequencies. The same input parameter set as for Fig 2D and 2E was used. The threshold was fixed to 8 inputs in C.
Mentions: Simulated rate-MTF curves of the pure integrator showed a broad tuning (Fig 14A), which resembles the all-pass property of input fibers (Fig 2A). The response rates were slightly reduced at low frequencies (< 300 Hz) where the refractory period plays a role. Simulated synch-MTFs of the pure integrator showed a high gain (> 3 dB) for only a narrow range of modulation frequencies (Fig 14B). For other frequencies, gains were generally lower than the coincidence counting model (Fig 4D) and physiological data [36]. Thus the responses of the pure integrator were largely inconsistent with empirical LSO responses to monaural AM sounds (Fig 1A and [36]).

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