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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.


Spontaneous oscillatory activity is not synchronized across receptors.(A) Receptor locations on the right side of one P. tenuicauda are illustrated as black dots (receptor size not to scale). (B) An approximate map of all 36 receptors in the right augenrosette of one P. tenuicauda. This map comes from a different fish than shown in A. (C) Top, simultaneous extracellular recordings from a receptor in the left kehlrosette (black) and a receptor in the left augenrosette of one P. tenuicauda. Bottom, instantaneous oscillatory phases of the simultaneous recordings obtained through Hilbert transform of the recorded potentials. (D) The product of the individual probability distributions of instantaneous phases from the same two receptors shown in C. The product of the individual probability distributions from each of five separate 1-s recordings was calculated. The average product across these five recordings is shown. (E) The joint probability distribution of instantaneous phases of the two receptors shown in C and D. The joint probability distribution was calculated over five separate 1-s recordings and then averaged. (F) The joint probability distribution of instantaneous phases of the first of five recordings from one receptor and the last of five recordings from the other receptor, and vice versa. The joint probability distributions from these two non-simultaneous recording pairs were averaged. (G) Differential extracellular recordings from a position centered over the right nackenrosette (black) and a position 2 mm posterior (red) in one P. tenuicauda. The recording and reference terminals of the electrode were separated by 5 mm. (H) Power spectra for the differential recordings shown in G. Only the frequency range where peaks occurred is shown (∼1.7–2.1 kHz).DOI:http://dx.doi.org/10.7554/eLife.08163.004
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fig2: Spontaneous oscillatory activity is not synchronized across receptors.(A) Receptor locations on the right side of one P. tenuicauda are illustrated as black dots (receptor size not to scale). (B) An approximate map of all 36 receptors in the right augenrosette of one P. tenuicauda. This map comes from a different fish than shown in A. (C) Top, simultaneous extracellular recordings from a receptor in the left kehlrosette (black) and a receptor in the left augenrosette of one P. tenuicauda. Bottom, instantaneous oscillatory phases of the simultaneous recordings obtained through Hilbert transform of the recorded potentials. (D) The product of the individual probability distributions of instantaneous phases from the same two receptors shown in C. The product of the individual probability distributions from each of five separate 1-s recordings was calculated. The average product across these five recordings is shown. (E) The joint probability distribution of instantaneous phases of the two receptors shown in C and D. The joint probability distribution was calculated over five separate 1-s recordings and then averaged. (F) The joint probability distribution of instantaneous phases of the first of five recordings from one receptor and the last of five recordings from the other receptor, and vice versa. The joint probability distributions from these two non-simultaneous recording pairs were averaged. (G) Differential extracellular recordings from a position centered over the right nackenrosette (black) and a position 2 mm posterior (red) in one P. tenuicauda. The recording and reference terminals of the electrode were separated by 5 mm. (H) Power spectra for the differential recordings shown in G. Only the frequency range where peaks occurred is shown (∼1.7–2.1 kHz).DOI:http://dx.doi.org/10.7554/eLife.08163.004

Mentions: Oscillating receptors are organized into three rosettes on each side of the head (Figure 2A) (Harder, 1968b; Lavoue et al., 2004, 2010; Carlson et al., 2011). To study how spontaneous activity varied within a rosette, we obtained spontaneous recordings from every receptor in a single rosette in one Petrocephalus tenuicauda (Figure 2B). Spontaneous oscillation amplitude was largest in the center of the rosette and progressively decreased towards the periphery. Oscillation frequency and amplitude were not significantly correlated (Spearman R = 0.27, t(22) = 1.3, p = 0.21), although frequencies tended to be highest near the center of the rosette (Figure 2B).10.7554/eLife.08163.004Figure 2.Spontaneous oscillatory activity is not synchronized across receptors.


Peripheral sensory coding through oscillatory synchrony in weakly electric fish.

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

Spontaneous oscillatory activity is not synchronized across receptors.(A) Receptor locations on the right side of one P. tenuicauda are illustrated as black dots (receptor size not to scale). (B) An approximate map of all 36 receptors in the right augenrosette of one P. tenuicauda. This map comes from a different fish than shown in A. (C) Top, simultaneous extracellular recordings from a receptor in the left kehlrosette (black) and a receptor in the left augenrosette of one P. tenuicauda. Bottom, instantaneous oscillatory phases of the simultaneous recordings obtained through Hilbert transform of the recorded potentials. (D) The product of the individual probability distributions of instantaneous phases from the same two receptors shown in C. The product of the individual probability distributions from each of five separate 1-s recordings was calculated. The average product across these five recordings is shown. (E) The joint probability distribution of instantaneous phases of the two receptors shown in C and D. The joint probability distribution was calculated over five separate 1-s recordings and then averaged. (F) The joint probability distribution of instantaneous phases of the first of five recordings from one receptor and the last of five recordings from the other receptor, and vice versa. The joint probability distributions from these two non-simultaneous recording pairs were averaged. (G) Differential extracellular recordings from a position centered over the right nackenrosette (black) and a position 2 mm posterior (red) in one P. tenuicauda. The recording and reference terminals of the electrode were separated by 5 mm. (H) Power spectra for the differential recordings shown in G. Only the frequency range where peaks occurred is shown (∼1.7–2.1 kHz).DOI:http://dx.doi.org/10.7554/eLife.08163.004
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Related In: Results  -  Collection

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fig2: Spontaneous oscillatory activity is not synchronized across receptors.(A) Receptor locations on the right side of one P. tenuicauda are illustrated as black dots (receptor size not to scale). (B) An approximate map of all 36 receptors in the right augenrosette of one P. tenuicauda. This map comes from a different fish than shown in A. (C) Top, simultaneous extracellular recordings from a receptor in the left kehlrosette (black) and a receptor in the left augenrosette of one P. tenuicauda. Bottom, instantaneous oscillatory phases of the simultaneous recordings obtained through Hilbert transform of the recorded potentials. (D) The product of the individual probability distributions of instantaneous phases from the same two receptors shown in C. The product of the individual probability distributions from each of five separate 1-s recordings was calculated. The average product across these five recordings is shown. (E) The joint probability distribution of instantaneous phases of the two receptors shown in C and D. The joint probability distribution was calculated over five separate 1-s recordings and then averaged. (F) The joint probability distribution of instantaneous phases of the first of five recordings from one receptor and the last of five recordings from the other receptor, and vice versa. The joint probability distributions from these two non-simultaneous recording pairs were averaged. (G) Differential extracellular recordings from a position centered over the right nackenrosette (black) and a position 2 mm posterior (red) in one P. tenuicauda. The recording and reference terminals of the electrode were separated by 5 mm. (H) Power spectra for the differential recordings shown in G. Only the frequency range where peaks occurred is shown (∼1.7–2.1 kHz).DOI:http://dx.doi.org/10.7554/eLife.08163.004
Mentions: Oscillating receptors are organized into three rosettes on each side of the head (Figure 2A) (Harder, 1968b; Lavoue et al., 2004, 2010; Carlson et al., 2011). To study how spontaneous activity varied within a rosette, we obtained spontaneous recordings from every receptor in a single rosette in one Petrocephalus tenuicauda (Figure 2B). Spontaneous oscillation amplitude was largest in the center of the rosette and progressively decreased towards the periphery. Oscillation frequency and amplitude were not significantly correlated (Spearman R = 0.27, t(22) = 1.3, p = 0.21), although frequencies tended to be highest near the center of the rosette (Figure 2B).10.7554/eLife.08163.004Figure 2.Spontaneous oscillatory activity is not synchronized across receptors.

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.