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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

Recorded responses of cat LSO neurons to AM sounds.A: Monaural AM responses with varied modulation frequencies. Different lines are used for different LSO units. Several response types of AM-tuning were found and shown in different colors. Some units exhibited characteristics of multiple response types. B: Binaural AM responses with varied ITDs. Different line types correspond to different modulation frequencies. Adapted and redrawn from Figs 13B and 16B of Joris and Yin [36] with permission.
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pcbi.1004997.g001: Recorded responses of cat LSO neurons to AM sounds.A: Monaural AM responses with varied modulation frequencies. Different lines are used for different LSO units. Several response types of AM-tuning were found and shown in different colors. Some units exhibited characteristics of multiple response types. B: Binaural AM responses with varied ITDs. Different line types correspond to different modulation frequencies. Adapted and redrawn from Figs 13B and 16B of Joris and Yin [36] with permission.

Mentions: LSO responses to monaural AM tones at different modulation frequencies were systematically studied by Joris and Yin [36]. Typically, spike rates showed a mild peak at modulation frequencies (fm) of 100–500 Hz, and gradually decreased down to 50 spikes/sec at around fm = 600–1000 Hz (Fig 1A, blue lines). However, the variability of responses from neuron to neuron was unexpectedly large. Some LSO neurons showed monotonic decreases in spike rate along the modulation-frequency axis (Fig 1A, red lines) whereas spike rates of other units remained > 100 spikes/sec over the fm ranges tested (Fig 1A, green lines). A few LSO neurons showed low spike rates for monaural AM sounds (Fig 1A, orange lines). Joris and Yin [36] suggested that the low-pass nature of LSO rate tuning was likely not inherited from their inputs from spherical bushy cell in the VCN, because the firing rates of bushy cells were more stable (i.e., all-pass) with increasing fm than LSO neurons. The source of the variability in AM rate coding should thus originate at the synaptic and membrane levels of the LSO neuron, making a contrast to frequency tuning in the inferior colliculus that inherits and combines a variation of spectral tuning patterns of ascending projections [37,38]. Wang and Colburn [39] studied LSO responses to AM sounds, using detailed conductance-based models. Their series of simulations suggested that the membrane afterhyperpolarization, which was shown to be important for the characteristic ‘chopping’ responses of LSO to pure tone stimuli [18], was unlikely to be the primary mechanism for rate decreases in AM coding with increasing fm, whereas the addition of a large amount of low-voltage-activated potassium (KLVA) conductance led to rate-fm functions that were more consistent with empirical results. Nevertheless, no combinations of parameters were able to comprehensively explain the diversity of LSO responses to monaural AM stimuli.


Roles for Coincidence Detection in Coding Amplitude-Modulated Sounds.

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

Recorded responses of cat LSO neurons to AM sounds.A: Monaural AM responses with varied modulation frequencies. Different lines are used for different LSO units. Several response types of AM-tuning were found and shown in different colors. Some units exhibited characteristics of multiple response types. B: Binaural AM responses with varied ITDs. Different line types correspond to different modulation frequencies. Adapted and redrawn from Figs 13B and 16B of Joris and Yin [36] with permission.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4920552&req=5

pcbi.1004997.g001: Recorded responses of cat LSO neurons to AM sounds.A: Monaural AM responses with varied modulation frequencies. Different lines are used for different LSO units. Several response types of AM-tuning were found and shown in different colors. Some units exhibited characteristics of multiple response types. B: Binaural AM responses with varied ITDs. Different line types correspond to different modulation frequencies. Adapted and redrawn from Figs 13B and 16B of Joris and Yin [36] with permission.
Mentions: LSO responses to monaural AM tones at different modulation frequencies were systematically studied by Joris and Yin [36]. Typically, spike rates showed a mild peak at modulation frequencies (fm) of 100–500 Hz, and gradually decreased down to 50 spikes/sec at around fm = 600–1000 Hz (Fig 1A, blue lines). However, the variability of responses from neuron to neuron was unexpectedly large. Some LSO neurons showed monotonic decreases in spike rate along the modulation-frequency axis (Fig 1A, red lines) whereas spike rates of other units remained > 100 spikes/sec over the fm ranges tested (Fig 1A, green lines). A few LSO neurons showed low spike rates for monaural AM sounds (Fig 1A, orange lines). Joris and Yin [36] suggested that the low-pass nature of LSO rate tuning was likely not inherited from their inputs from spherical bushy cell in the VCN, because the firing rates of bushy cells were more stable (i.e., all-pass) with increasing fm than LSO neurons. The source of the variability in AM rate coding should thus originate at the synaptic and membrane levels of the LSO neuron, making a contrast to frequency tuning in the inferior colliculus that inherits and combines a variation of spectral tuning patterns of ascending projections [37,38]. Wang and Colburn [39] studied LSO responses to AM sounds, using detailed conductance-based models. Their series of simulations suggested that the membrane afterhyperpolarization, which was shown to be important for the characteristic ‘chopping’ responses of LSO to pure tone stimuli [18], was unlikely to be the primary mechanism for rate decreases in AM coding with increasing fm, whereas the addition of a large amount of low-voltage-activated potassium (KLVA) conductance led to rate-fm functions that were more consistent with empirical results. Nevertheless, no combinations of parameters were able to comprehensively explain the diversity of LSO responses to monaural AM stimuli.

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