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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 are most sensitive to submillisecond IPIs occurring in group communication signals.(A) A histogram of the IPIs recorded over 20 min from a single fish with spiking receptors (P. microphthalmus). Inset, illustration of IPI calculation. We recorded the electric signaling activity from a single fish and recorded the time of each EOD as the time at which the rectified potential crossed a predefined threshold (tick marks above electrical recording trace). We then calculated IPIs as the time between successive EODs. (B) Same as A for a recording from a group tank of 24 P. microphthalmus. Inset, electrical recording from the same group of fish illustrating submillisecond IPIs. EOD polarity and amplitude depend on fish's orientation and location relative to the recording electrode. (C) Spike probability of three P. microphthalmus receptors (green; y-axis on right; same data as in Figure 5C) vs IPI superimposed on the IPI histogram from B. Note the expanded data range in the x-axis. Each point represents the mean across three receptors and error bars represent S.E.M. (D, E) Same as in A and B for a congeneric species with oscillating receptors (P. tenuicauda). (F) Normalized oscillation amplitudes of three P. tenuicauda receptors (black; y-axis on right; same data as in Figure 6C at 10 nA) vs IPI superimposed on the IPI histogram from E. Note the expanded data range in the x-axis. Each point represents the mean across three receptors and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.08163.010
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fig8: Oscillating receptors are most sensitive to submillisecond IPIs occurring in group communication signals.(A) A histogram of the IPIs recorded over 20 min from a single fish with spiking receptors (P. microphthalmus). Inset, illustration of IPI calculation. We recorded the electric signaling activity from a single fish and recorded the time of each EOD as the time at which the rectified potential crossed a predefined threshold (tick marks above electrical recording trace). We then calculated IPIs as the time between successive EODs. (B) Same as A for a recording from a group tank of 24 P. microphthalmus. Inset, electrical recording from the same group of fish illustrating submillisecond IPIs. EOD polarity and amplitude depend on fish's orientation and location relative to the recording electrode. (C) Spike probability of three P. microphthalmus receptors (green; y-axis on right; same data as in Figure 5C) vs IPI superimposed on the IPI histogram from B. Note the expanded data range in the x-axis. Each point represents the mean across three receptors and error bars represent S.E.M. (D, E) Same as in A and B for a congeneric species with oscillating receptors (P. tenuicauda). (F) Normalized oscillation amplitudes of three P. tenuicauda receptors (black; y-axis on right; same data as in Figure 6C at 10 nA) vs IPI superimposed on the IPI histogram from E. Note the expanded data range in the x-axis. Each point represents the mean across three receptors and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.08163.010

Mentions: Even though the minimum IPI a single fish produces is approximately 8 ms, a large group of signaling fish may collectively produce much shorter IPIs. Could the oscillations in rosette receptors be tuned to these shorter IPIs? To test this hypothesis, we first recorded 20 min of electric signaling from individual fish of a species with spiking receptors (P. microphthalmus) (e.g., Figure 8A) and from individual fish of a congeneric species with oscillating receptors (P. tenuicauda) (e.g., Figure 8D). Next, we recorded electrical activity from group tanks of each of the same two species (Figure 8B,E). Indeed, group signals contained much shorter IPIs than single-fish signals (compare Figure 8B with Figure 8A, and Figure 8E with Figure 8D; note different time scales).10.7554/eLife.08163.010Figure 8.Oscillating receptors are most sensitive to submillisecond IPIs occurring in group communication signals.


Peripheral sensory coding through oscillatory synchrony in weakly electric fish.

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

Oscillating receptors are most sensitive to submillisecond IPIs occurring in group communication signals.(A) A histogram of the IPIs recorded over 20 min from a single fish with spiking receptors (P. microphthalmus). Inset, illustration of IPI calculation. We recorded the electric signaling activity from a single fish and recorded the time of each EOD as the time at which the rectified potential crossed a predefined threshold (tick marks above electrical recording trace). We then calculated IPIs as the time between successive EODs. (B) Same as A for a recording from a group tank of 24 P. microphthalmus. Inset, electrical recording from the same group of fish illustrating submillisecond IPIs. EOD polarity and amplitude depend on fish's orientation and location relative to the recording electrode. (C) Spike probability of three P. microphthalmus receptors (green; y-axis on right; same data as in Figure 5C) vs IPI superimposed on the IPI histogram from B. Note the expanded data range in the x-axis. Each point represents the mean across three receptors and error bars represent S.E.M. (D, E) Same as in A and B for a congeneric species with oscillating receptors (P. tenuicauda). (F) Normalized oscillation amplitudes of three P. tenuicauda receptors (black; y-axis on right; same data as in Figure 6C at 10 nA) vs IPI superimposed on the IPI histogram from E. Note the expanded data range in the x-axis. Each point represents the mean across three receptors and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.08163.010
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fig8: Oscillating receptors are most sensitive to submillisecond IPIs occurring in group communication signals.(A) A histogram of the IPIs recorded over 20 min from a single fish with spiking receptors (P. microphthalmus). Inset, illustration of IPI calculation. We recorded the electric signaling activity from a single fish and recorded the time of each EOD as the time at which the rectified potential crossed a predefined threshold (tick marks above electrical recording trace). We then calculated IPIs as the time between successive EODs. (B) Same as A for a recording from a group tank of 24 P. microphthalmus. Inset, electrical recording from the same group of fish illustrating submillisecond IPIs. EOD polarity and amplitude depend on fish's orientation and location relative to the recording electrode. (C) Spike probability of three P. microphthalmus receptors (green; y-axis on right; same data as in Figure 5C) vs IPI superimposed on the IPI histogram from B. Note the expanded data range in the x-axis. Each point represents the mean across three receptors and error bars represent S.E.M. (D, E) Same as in A and B for a congeneric species with oscillating receptors (P. tenuicauda). (F) Normalized oscillation amplitudes of three P. tenuicauda receptors (black; y-axis on right; same data as in Figure 6C at 10 nA) vs IPI superimposed on the IPI histogram from E. Note the expanded data range in the x-axis. Each point represents the mean across three receptors and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.08163.010
Mentions: Even though the minimum IPI a single fish produces is approximately 8 ms, a large group of signaling fish may collectively produce much shorter IPIs. Could the oscillations in rosette receptors be tuned to these shorter IPIs? To test this hypothesis, we first recorded 20 min of electric signaling from individual fish of a species with spiking receptors (P. microphthalmus) (e.g., Figure 8A) and from individual fish of a congeneric species with oscillating receptors (P. tenuicauda) (e.g., Figure 8D). Next, we recorded electrical activity from group tanks of each of the same two species (Figure 8B,E). Indeed, group signals contained much shorter IPIs than single-fish signals (compare Figure 8B with Figure 8A, and Figure 8E with Figure 8D; note different time scales).10.7554/eLife.08163.010Figure 8.Oscillating receptors are most sensitive to submillisecond IPIs occurring in group communication signals.

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.