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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.


Frequency sensitivity of spiking receptors is matched to conspecific EOD power spectra, whereas frequency sensitivity of oscillating receptors is not.(A) Representative EODs from four species with spiking receptors (Brienomyrus brachyistius, P. microphthalmus, Brevimyrus niger, and Pollimyrus adspersus), and two species with oscillating receptors (P. tenuicauda and P. soudanensis), plotted head-positive up with normalized peak-to-peak heights. (B, C) Average power spectra of EODs from species with spiking receptors (B) and from species with oscillating receptors (C). (D) Frequency tuning curves for representative spiking receptors from four species. Threshold was determined as the lowest intensity stimulus that elicited a spiking response. The frequency with the lowest threshold was taken as the receptor's best frequency. Thresholds were defined as dB relative to the threshold at each receptor's best frequency. Open symbols indicate stimuli for which there was no response from the receptor at the intensity shown, but responses to higher intensities were not recorded. (E) Frequency tuning curves for a representative oscillating receptor from P. tenuicauda at three intensities. Stimuli were single-cycle bipolar sine waves with positive polarity (peak preceding trough). Vector strength was used as a measure of phase-locking across responses. Vector strength equals 1 when the phase of the oscillatory reset is the same for each stimulus presentation and 0 when the phase of oscillatory reset is completely random for each stimulus presentation. The frequency that elicited the highest vector strength was taken as each receptor's best frequency. (F) Average receptor best frequency vs average conspecific EOD peak power frequency for all species studied. Best frequencies were averaged across responses to positive- and negative- (trough preceding peak) polarity stimuli in oscillating receptors. We used the best frequencies at 10 nA in P. tenuicauda. Closed symbols denote species with spiking receptors and open symbols denote species with oscillating receptors. (G) Vector strength of oscillating responses to positive-polarity single-cycle bipolar sine stimuli at multiples of receptors' spontaneous oscillation periods at three intensities in P. tenuicauda. Each point in F and G represents the average across receptors where appropriate, and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.08163.006
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fig4: Frequency sensitivity of spiking receptors is matched to conspecific EOD power spectra, whereas frequency sensitivity of oscillating receptors is not.(A) Representative EODs from four species with spiking receptors (Brienomyrus brachyistius, P. microphthalmus, Brevimyrus niger, and Pollimyrus adspersus), and two species with oscillating receptors (P. tenuicauda and P. soudanensis), plotted head-positive up with normalized peak-to-peak heights. (B, C) Average power spectra of EODs from species with spiking receptors (B) and from species with oscillating receptors (C). (D) Frequency tuning curves for representative spiking receptors from four species. Threshold was determined as the lowest intensity stimulus that elicited a spiking response. The frequency with the lowest threshold was taken as the receptor's best frequency. Thresholds were defined as dB relative to the threshold at each receptor's best frequency. Open symbols indicate stimuli for which there was no response from the receptor at the intensity shown, but responses to higher intensities were not recorded. (E) Frequency tuning curves for a representative oscillating receptor from P. tenuicauda at three intensities. Stimuli were single-cycle bipolar sine waves with positive polarity (peak preceding trough). Vector strength was used as a measure of phase-locking across responses. Vector strength equals 1 when the phase of the oscillatory reset is the same for each stimulus presentation and 0 when the phase of oscillatory reset is completely random for each stimulus presentation. The frequency that elicited the highest vector strength was taken as each receptor's best frequency. (F) Average receptor best frequency vs average conspecific EOD peak power frequency for all species studied. Best frequencies were averaged across responses to positive- and negative- (trough preceding peak) polarity stimuli in oscillating receptors. We used the best frequencies at 10 nA in P. tenuicauda. Closed symbols denote species with spiking receptors and open symbols denote species with oscillating receptors. (G) Vector strength of oscillating responses to positive-polarity single-cycle bipolar sine stimuli at multiples of receptors' spontaneous oscillation periods at three intensities in P. tenuicauda. Each point in F and G represents the average across receptors where appropriate, and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.08163.006

Mentions: Spiking receptors have been reported to be most sensitive to the frequencies occurring in conspecific EOD waveforms (Hopkins, 1981; Bass and Hopkins, 1984; Lyons-Warren et al., 2012). To confirm this finding in our test species, we compared the frequency sensitivity of individual spiking receptors to the power spectra of conspecific EODs (Figure 4A,B,D). We collected threshold frequency tuning curves as described previously (Lyons-Warren et al., 2012). We defined a receptor's best frequency as the frequency with the lowest threshold. In general, spiking receptors had best frequencies that were close to the frequencies with the highest power in conspecific EODs (compare Figure 4D with Figure 4B). On average, the best frequencies of spiking receptors were within one octave of the peak power frequencies of conspecific EODs (filled symbols in Figure 4F).10.7554/eLife.08163.006Figure 4.Frequency sensitivity of spiking receptors is matched to conspecific EOD power spectra, whereas frequency sensitivity of oscillating receptors is not.


Peripheral sensory coding through oscillatory synchrony in weakly electric fish.

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

Frequency sensitivity of spiking receptors is matched to conspecific EOD power spectra, whereas frequency sensitivity of oscillating receptors is not.(A) Representative EODs from four species with spiking receptors (Brienomyrus brachyistius, P. microphthalmus, Brevimyrus niger, and Pollimyrus adspersus), and two species with oscillating receptors (P. tenuicauda and P. soudanensis), plotted head-positive up with normalized peak-to-peak heights. (B, C) Average power spectra of EODs from species with spiking receptors (B) and from species with oscillating receptors (C). (D) Frequency tuning curves for representative spiking receptors from four species. Threshold was determined as the lowest intensity stimulus that elicited a spiking response. The frequency with the lowest threshold was taken as the receptor's best frequency. Thresholds were defined as dB relative to the threshold at each receptor's best frequency. Open symbols indicate stimuli for which there was no response from the receptor at the intensity shown, but responses to higher intensities were not recorded. (E) Frequency tuning curves for a representative oscillating receptor from P. tenuicauda at three intensities. Stimuli were single-cycle bipolar sine waves with positive polarity (peak preceding trough). Vector strength was used as a measure of phase-locking across responses. Vector strength equals 1 when the phase of the oscillatory reset is the same for each stimulus presentation and 0 when the phase of oscillatory reset is completely random for each stimulus presentation. The frequency that elicited the highest vector strength was taken as each receptor's best frequency. (F) Average receptor best frequency vs average conspecific EOD peak power frequency for all species studied. Best frequencies were averaged across responses to positive- and negative- (trough preceding peak) polarity stimuli in oscillating receptors. We used the best frequencies at 10 nA in P. tenuicauda. Closed symbols denote species with spiking receptors and open symbols denote species with oscillating receptors. (G) Vector strength of oscillating responses to positive-polarity single-cycle bipolar sine stimuli at multiples of receptors' spontaneous oscillation periods at three intensities in P. tenuicauda. Each point in F and G represents the average across receptors where appropriate, and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.08163.006
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fig4: Frequency sensitivity of spiking receptors is matched to conspecific EOD power spectra, whereas frequency sensitivity of oscillating receptors is not.(A) Representative EODs from four species with spiking receptors (Brienomyrus brachyistius, P. microphthalmus, Brevimyrus niger, and Pollimyrus adspersus), and two species with oscillating receptors (P. tenuicauda and P. soudanensis), plotted head-positive up with normalized peak-to-peak heights. (B, C) Average power spectra of EODs from species with spiking receptors (B) and from species with oscillating receptors (C). (D) Frequency tuning curves for representative spiking receptors from four species. Threshold was determined as the lowest intensity stimulus that elicited a spiking response. The frequency with the lowest threshold was taken as the receptor's best frequency. Thresholds were defined as dB relative to the threshold at each receptor's best frequency. Open symbols indicate stimuli for which there was no response from the receptor at the intensity shown, but responses to higher intensities were not recorded. (E) Frequency tuning curves for a representative oscillating receptor from P. tenuicauda at three intensities. Stimuli were single-cycle bipolar sine waves with positive polarity (peak preceding trough). Vector strength was used as a measure of phase-locking across responses. Vector strength equals 1 when the phase of the oscillatory reset is the same for each stimulus presentation and 0 when the phase of oscillatory reset is completely random for each stimulus presentation. The frequency that elicited the highest vector strength was taken as each receptor's best frequency. (F) Average receptor best frequency vs average conspecific EOD peak power frequency for all species studied. Best frequencies were averaged across responses to positive- and negative- (trough preceding peak) polarity stimuli in oscillating receptors. We used the best frequencies at 10 nA in P. tenuicauda. Closed symbols denote species with spiking receptors and open symbols denote species with oscillating receptors. (G) Vector strength of oscillating responses to positive-polarity single-cycle bipolar sine stimuli at multiples of receptors' spontaneous oscillation periods at three intensities in P. tenuicauda. Each point in F and G represents the average across receptors where appropriate, and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.08163.006
Mentions: Spiking receptors have been reported to be most sensitive to the frequencies occurring in conspecific EOD waveforms (Hopkins, 1981; Bass and Hopkins, 1984; Lyons-Warren et al., 2012). To confirm this finding in our test species, we compared the frequency sensitivity of individual spiking receptors to the power spectra of conspecific EODs (Figure 4A,B,D). We collected threshold frequency tuning curves as described previously (Lyons-Warren et al., 2012). We defined a receptor's best frequency as the frequency with the lowest threshold. In general, spiking receptors had best frequencies that were close to the frequencies with the highest power in conspecific EODs (compare Figure 4D with Figure 4B). On average, the best frequencies of spiking receptors were within one octave of the peak power frequencies of conspecific EODs (filled symbols in Figure 4F).10.7554/eLife.08163.006Figure 4.Frequency sensitivity of spiking receptors is matched to conspecific EOD power spectra, whereas frequency sensitivity of oscillating receptors is not.

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.