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Peripheral sensory coding through oscillatory synchrony in weakly electric fish.

Baker CA, Huck KR, Carlson BA - Elife (2015)

Bottom Line: We found that oscillating receptors respond to electric pulses by resetting their phase, resulting in transient synchrony among receptors that encodes signal timing and location, but not waveform.These receptors were most sensitive to frequencies found only in the collective signals of groups of conspecifics, and this was correlated with increased behavioral responses to these frequencies.Our findings provide the first evidence for sensory coding through oscillatory synchrony.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Washington University in St. Louis, St. Louis, United States.

ABSTRACT
Adaptations to an organism's environment often involve sensory system modifications. In this study, we address how evolutionary divergence in sensory perception relates to the physiological coding of stimuli. Mormyrid fishes that can detect subtle variations in electric communication signals encode signal waveform into spike-timing differences between sensory receptors. In contrast, the receptors of species insensitive to waveform variation produce spontaneously oscillating potentials. We found that oscillating receptors respond to electric pulses by resetting their phase, resulting in transient synchrony among receptors that encodes signal timing and location, but not waveform. These receptors were most sensitive to frequencies found only in the collective signals of groups of conspecifics, and this was correlated with increased behavioral responses to these frequencies. Thus, different perceptual capabilities correspond to different receptor physiologies. We hypothesize that these divergent mechanisms represent adaptations for different social environments. Our findings provide the first evidence for sensory coding through oscillatory synchrony.

No MeSH data available.


Oscillating receptors produce enhanced oscillation amplitudes at submillisecond IPIs matching their intrinsic oscillation periods.(A, B) Extracellular recording from an oscillating receptor in P. tenuicauda in response to a pair of monopolar square pulses of 0.2-ms duration and 0.50-ms IPI (A) and 5.0-ms IPI (B). We measured the oscillation amplitude on each stimulus presentation as the mean voltage of the first two poststimulus oscillatory peaks minus the voltage at the intervening trough. We then averaged amplitudes across all presentations of the same stimulus. (C) Oscillation amplitude evoked by the second pulse in the pair normalized to the amplitude evoked by a single pulse vs IPI for the responses of P. tenuicauda receptors at three stimulus intensities. Data shown are for positive-polarity pulses. (D) Same as C for IPIs corresponding to multiples of oscillating receptors' intrinsic oscillation periods. (E) Vector strength vs IPI for oscillating responses to positive-polarity stimuli at three intensities in the same receptors shown in C and D. (F) Same as E for IPIs corresponding to multiples of oscillating receptors' intrinsic oscillation periods for the same receptors shown in C–E. Each point in C–F represents the mean across receptors and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.08163.009
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fig7: Oscillating receptors produce enhanced oscillation amplitudes at submillisecond IPIs matching their intrinsic oscillation periods.(A, B) Extracellular recording from an oscillating receptor in P. tenuicauda in response to a pair of monopolar square pulses of 0.2-ms duration and 0.50-ms IPI (A) and 5.0-ms IPI (B). We measured the oscillation amplitude on each stimulus presentation as the mean voltage of the first two poststimulus oscillatory peaks minus the voltage at the intervening trough. We then averaged amplitudes across all presentations of the same stimulus. (C) Oscillation amplitude evoked by the second pulse in the pair normalized to the amplitude evoked by a single pulse vs IPI for the responses of P. tenuicauda receptors at three stimulus intensities. Data shown are for positive-polarity pulses. (D) Same as C for IPIs corresponding to multiples of oscillating receptors' intrinsic oscillation periods. (E) Vector strength vs IPI for oscillating responses to positive-polarity stimuli at three intensities in the same receptors shown in C and D. (F) Same as E for IPIs corresponding to multiples of oscillating receptors' intrinsic oscillation periods for the same receptors shown in C–E. Each point in C–F represents the mean across receptors and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.08163.009

Mentions: Oscillating receptors also encoded IPI into amplitude changes (Figure 7A,B). At the highest intensity tested, oscillation amplitudes were attenuated relative to single-pulse responses for IPIs below 1 ms (black curve in Figure 7C). As stimulus intensity decreased, however, oscillation amplitudes became selectively enhanced in response to 0.5-ms IPIs (Figure 7C). Phase-locking, as measured by the vector strength of oscillatory responses to the second pulse in the pair, also depended on IPI and stimulus intensity (Figure 7E). As the intensity decreased, responses became more sharply selective for IPIs around 0.5 ms, which is near the intrinsic oscillation periods (0.47–0.99 ms) of receptors in this species. This is suggestive of resonance in which stimulating an oscillating receptor with a pair of pulses separated by the receptor's intrinsic oscillation period results in stronger responses.10.7554/eLife.08163.009Figure 7.Oscillating receptors produce enhanced oscillation amplitudes at submillisecond IPIs matching their intrinsic oscillation periods.


Peripheral sensory coding through oscillatory synchrony in weakly electric fish.

Baker CA, Huck KR, Carlson BA - Elife (2015)

Oscillating receptors produce enhanced oscillation amplitudes at submillisecond IPIs matching their intrinsic oscillation periods.(A, B) Extracellular recording from an oscillating receptor in P. tenuicauda in response to a pair of monopolar square pulses of 0.2-ms duration and 0.50-ms IPI (A) and 5.0-ms IPI (B). We measured the oscillation amplitude on each stimulus presentation as the mean voltage of the first two poststimulus oscillatory peaks minus the voltage at the intervening trough. We then averaged amplitudes across all presentations of the same stimulus. (C) Oscillation amplitude evoked by the second pulse in the pair normalized to the amplitude evoked by a single pulse vs IPI for the responses of P. tenuicauda receptors at three stimulus intensities. Data shown are for positive-polarity pulses. (D) Same as C for IPIs corresponding to multiples of oscillating receptors' intrinsic oscillation periods. (E) Vector strength vs IPI for oscillating responses to positive-polarity stimuli at three intensities in the same receptors shown in C and D. (F) Same as E for IPIs corresponding to multiples of oscillating receptors' intrinsic oscillation periods for the same receptors shown in C–E. Each point in C–F represents the mean across receptors and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.08163.009
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fig7: Oscillating receptors produce enhanced oscillation amplitudes at submillisecond IPIs matching their intrinsic oscillation periods.(A, B) Extracellular recording from an oscillating receptor in P. tenuicauda in response to a pair of monopolar square pulses of 0.2-ms duration and 0.50-ms IPI (A) and 5.0-ms IPI (B). We measured the oscillation amplitude on each stimulus presentation as the mean voltage of the first two poststimulus oscillatory peaks minus the voltage at the intervening trough. We then averaged amplitudes across all presentations of the same stimulus. (C) Oscillation amplitude evoked by the second pulse in the pair normalized to the amplitude evoked by a single pulse vs IPI for the responses of P. tenuicauda receptors at three stimulus intensities. Data shown are for positive-polarity pulses. (D) Same as C for IPIs corresponding to multiples of oscillating receptors' intrinsic oscillation periods. (E) Vector strength vs IPI for oscillating responses to positive-polarity stimuli at three intensities in the same receptors shown in C and D. (F) Same as E for IPIs corresponding to multiples of oscillating receptors' intrinsic oscillation periods for the same receptors shown in C–E. Each point in C–F represents the mean across receptors and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.08163.009
Mentions: Oscillating receptors also encoded IPI into amplitude changes (Figure 7A,B). At the highest intensity tested, oscillation amplitudes were attenuated relative to single-pulse responses for IPIs below 1 ms (black curve in Figure 7C). As stimulus intensity decreased, however, oscillation amplitudes became selectively enhanced in response to 0.5-ms IPIs (Figure 7C). Phase-locking, as measured by the vector strength of oscillatory responses to the second pulse in the pair, also depended on IPI and stimulus intensity (Figure 7E). As the intensity decreased, responses became more sharply selective for IPIs around 0.5 ms, which is near the intrinsic oscillation periods (0.47–0.99 ms) of receptors in this species. This is suggestive of resonance in which stimulating an oscillating receptor with a pair of pulses separated by the receptor's intrinsic oscillation period results in stronger responses.10.7554/eLife.08163.009Figure 7.Oscillating receptors produce enhanced oscillation amplitudes at submillisecond IPIs matching their intrinsic oscillation periods.

Bottom Line: We found that oscillating receptors respond to electric pulses by resetting their phase, resulting in transient synchrony among receptors that encodes signal timing and location, but not waveform.These receptors were most sensitive to frequencies found only in the collective signals of groups of conspecifics, and this was correlated with increased behavioral responses to these frequencies.Our findings provide the first evidence for sensory coding through oscillatory synchrony.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Washington University in St. Louis, St. Louis, United States.

ABSTRACT
Adaptations to an organism's environment often involve sensory system modifications. In this study, we address how evolutionary divergence in sensory perception relates to the physiological coding of stimuli. Mormyrid fishes that can detect subtle variations in electric communication signals encode signal waveform into spike-timing differences between sensory receptors. In contrast, the receptors of species insensitive to waveform variation produce spontaneously oscillating potentials. We found that oscillating receptors respond to electric pulses by resetting their phase, resulting in transient synchrony among receptors that encodes signal timing and location, but not waveform. These receptors were most sensitive to frequencies found only in the collective signals of groups of conspecifics, and this was correlated with increased behavioral responses to these frequencies. Thus, different perceptual capabilities correspond to different receptor physiologies. We hypothesize that these divergent mechanisms represent adaptations for different social environments. Our findings provide the first evidence for sensory coding through oscillatory synchrony.

No MeSH data available.