Limits...
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.


Spiking receptors encode pulse duration, whereas oscillating receptors do not.(A, B) Extracellular recordings from a spiking receptor in B. niger during stimulation with positive-polarity (black) and negative-polarity (red) monopolar square pulses of 0.10-ms duration (A) and 0.2-ms duration (B). In both cases, the difference in spike times (Δt) matches the pulse duration. Traces from five stimulus repetitions are superimposed. (C) Spike probability vs square pulse duration for responses to positive-polarity stimuli for spiking receptors of three species. Horizontal bars indicate the behaviorally relevant ranges of total durations measured in 10 conspecific electric organ discharge (EOD) waveforms. (D) Spike-timing differences between responses to positive- and negative-polarity stimuli vs square pulse duration for the same receptors in C. (E, F) Extracellular recordings from an oscillating receptor in P. tenuicauda during stimulation with positive- (black) and negative- (red) polarity monopolar square pulses of 0.10-ms duration (E) and 0.20-ms duration (F). In both cases, the timing difference (Δt) between oscillatory peaks elicited by opposite-polarity stimuli does not match the pulse duration. Traces from five stimulus repetitions are superimposed. (G) Evoked oscillation amplitudes normalized to prestimulus oscillation amplitudes vs square pulse duration for oscillating receptors. Curves for each receptor are shown in gray, and the averages across receptors are shown in black. The horizontal bar indicates the range of total durations of 10 conspecific EODs. (H) Oscillation-timing differences between responses to positive- and negative-polarity stimuli vs square pulse duration for the same receptors shown in G. (I, J) Extracellular recordings from an oscillating receptor in P. tenuicauda in response to a head-positive (‘normal polarity’) conspecific EOD waveform (black) and the reverse-polarity waveform (red) at an intensity of 316 nA (I) and 32 nA (J). Traces from five stimulus repetitions are superimposed. (K) Vector strength vs phase difference of oscillatory responses to opposite-polarity conspecific EODs in P. tenuicauda. Each point represents the mean of responses from six receptors. Vector strength was averaged across stimulus polarity within each receptor before averaging across receptors. Error bars represent S.E.M. Closed circles indicate phase resets that were significantly different for normal- vs reversed-polarity EODs (Hotelling test for paired circular data, F > Fcrit = 6.9, p < 0.05). The stimulus intensities that evoked significantly different phase resets for opposite polarity EODs were 56, 178, and 316 nA. Intensities of 100 nA and <56 nA did not result in significantly different phase resets. (L) Phase differences between responses to positive- and negative-polarity stimuli vs square pulse duration for oscillatory responses to monopolar square electric pulses.DOI:http://dx.doi.org/10.7554/eLife.08163.005
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4522468&req=5

fig3: Spiking receptors encode pulse duration, whereas oscillating receptors do not.(A, B) Extracellular recordings from a spiking receptor in B. niger during stimulation with positive-polarity (black) and negative-polarity (red) monopolar square pulses of 0.10-ms duration (A) and 0.2-ms duration (B). In both cases, the difference in spike times (Δt) matches the pulse duration. Traces from five stimulus repetitions are superimposed. (C) Spike probability vs square pulse duration for responses to positive-polarity stimuli for spiking receptors of three species. Horizontal bars indicate the behaviorally relevant ranges of total durations measured in 10 conspecific electric organ discharge (EOD) waveforms. (D) Spike-timing differences between responses to positive- and negative-polarity stimuli vs square pulse duration for the same receptors in C. (E, F) Extracellular recordings from an oscillating receptor in P. tenuicauda during stimulation with positive- (black) and negative- (red) polarity monopolar square pulses of 0.10-ms duration (E) and 0.20-ms duration (F). In both cases, the timing difference (Δt) between oscillatory peaks elicited by opposite-polarity stimuli does not match the pulse duration. Traces from five stimulus repetitions are superimposed. (G) Evoked oscillation amplitudes normalized to prestimulus oscillation amplitudes vs square pulse duration for oscillating receptors. Curves for each receptor are shown in gray, and the averages across receptors are shown in black. The horizontal bar indicates the range of total durations of 10 conspecific EODs. (H) Oscillation-timing differences between responses to positive- and negative-polarity stimuli vs square pulse duration for the same receptors shown in G. (I, J) Extracellular recordings from an oscillating receptor in P. tenuicauda in response to a head-positive (‘normal polarity’) conspecific EOD waveform (black) and the reverse-polarity waveform (red) at an intensity of 316 nA (I) and 32 nA (J). Traces from five stimulus repetitions are superimposed. (K) Vector strength vs phase difference of oscillatory responses to opposite-polarity conspecific EODs in P. tenuicauda. Each point represents the mean of responses from six receptors. Vector strength was averaged across stimulus polarity within each receptor before averaging across receptors. Error bars represent S.E.M. Closed circles indicate phase resets that were significantly different for normal- vs reversed-polarity EODs (Hotelling test for paired circular data, F > Fcrit = 6.9, p < 0.05). The stimulus intensities that evoked significantly different phase resets for opposite polarity EODs were 56, 178, and 316 nA. Intensities of 100 nA and <56 nA did not result in significantly different phase resets. (L) Phase differences between responses to positive- and negative-polarity stimuli vs square pulse duration for oscillatory responses to monopolar square electric pulses.DOI:http://dx.doi.org/10.7554/eLife.08163.005

Mentions: To understand sensory encoding by these receptors, we recorded responses to focal stimulation with monopolar square pulses (Figure 3). We delivered both positive- and negative-polarity pulses to mimic the stimulation that receptors at different locations on the fish's body would experience during a natural global stimulus (Hopkins and Bass, 1981). As shown previously, spiking receptors responded with a single time-locked spike in response to inward current transients (Bennett, 1965), which occur at the onset of a positive-polarity pulse and at the offset of a negative-polarity pulse (Figure 3A,B). Spike probability depended on pulse duration (Figure 3C) but was high for stimulus durations within the range of total durations of conspecific EODs (horizontal bars in Figure 3C).10.7554/eLife.08163.005Figure 3.Spiking receptors encode pulse duration, whereas oscillating receptors do not.


Peripheral sensory coding through oscillatory synchrony in weakly electric fish.

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

Spiking receptors encode pulse duration, whereas oscillating receptors do not.(A, B) Extracellular recordings from a spiking receptor in B. niger during stimulation with positive-polarity (black) and negative-polarity (red) monopolar square pulses of 0.10-ms duration (A) and 0.2-ms duration (B). In both cases, the difference in spike times (Δt) matches the pulse duration. Traces from five stimulus repetitions are superimposed. (C) Spike probability vs square pulse duration for responses to positive-polarity stimuli for spiking receptors of three species. Horizontal bars indicate the behaviorally relevant ranges of total durations measured in 10 conspecific electric organ discharge (EOD) waveforms. (D) Spike-timing differences between responses to positive- and negative-polarity stimuli vs square pulse duration for the same receptors in C. (E, F) Extracellular recordings from an oscillating receptor in P. tenuicauda during stimulation with positive- (black) and negative- (red) polarity monopolar square pulses of 0.10-ms duration (E) and 0.20-ms duration (F). In both cases, the timing difference (Δt) between oscillatory peaks elicited by opposite-polarity stimuli does not match the pulse duration. Traces from five stimulus repetitions are superimposed. (G) Evoked oscillation amplitudes normalized to prestimulus oscillation amplitudes vs square pulse duration for oscillating receptors. Curves for each receptor are shown in gray, and the averages across receptors are shown in black. The horizontal bar indicates the range of total durations of 10 conspecific EODs. (H) Oscillation-timing differences between responses to positive- and negative-polarity stimuli vs square pulse duration for the same receptors shown in G. (I, J) Extracellular recordings from an oscillating receptor in P. tenuicauda in response to a head-positive (‘normal polarity’) conspecific EOD waveform (black) and the reverse-polarity waveform (red) at an intensity of 316 nA (I) and 32 nA (J). Traces from five stimulus repetitions are superimposed. (K) Vector strength vs phase difference of oscillatory responses to opposite-polarity conspecific EODs in P. tenuicauda. Each point represents the mean of responses from six receptors. Vector strength was averaged across stimulus polarity within each receptor before averaging across receptors. Error bars represent S.E.M. Closed circles indicate phase resets that were significantly different for normal- vs reversed-polarity EODs (Hotelling test for paired circular data, F > Fcrit = 6.9, p < 0.05). The stimulus intensities that evoked significantly different phase resets for opposite polarity EODs were 56, 178, and 316 nA. Intensities of 100 nA and <56 nA did not result in significantly different phase resets. (L) Phase differences between responses to positive- and negative-polarity stimuli vs square pulse duration for oscillatory responses to monopolar square electric pulses.DOI:http://dx.doi.org/10.7554/eLife.08163.005
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4522468&req=5

fig3: Spiking receptors encode pulse duration, whereas oscillating receptors do not.(A, B) Extracellular recordings from a spiking receptor in B. niger during stimulation with positive-polarity (black) and negative-polarity (red) monopolar square pulses of 0.10-ms duration (A) and 0.2-ms duration (B). In both cases, the difference in spike times (Δt) matches the pulse duration. Traces from five stimulus repetitions are superimposed. (C) Spike probability vs square pulse duration for responses to positive-polarity stimuli for spiking receptors of three species. Horizontal bars indicate the behaviorally relevant ranges of total durations measured in 10 conspecific electric organ discharge (EOD) waveforms. (D) Spike-timing differences between responses to positive- and negative-polarity stimuli vs square pulse duration for the same receptors in C. (E, F) Extracellular recordings from an oscillating receptor in P. tenuicauda during stimulation with positive- (black) and negative- (red) polarity monopolar square pulses of 0.10-ms duration (E) and 0.20-ms duration (F). In both cases, the timing difference (Δt) between oscillatory peaks elicited by opposite-polarity stimuli does not match the pulse duration. Traces from five stimulus repetitions are superimposed. (G) Evoked oscillation amplitudes normalized to prestimulus oscillation amplitudes vs square pulse duration for oscillating receptors. Curves for each receptor are shown in gray, and the averages across receptors are shown in black. The horizontal bar indicates the range of total durations of 10 conspecific EODs. (H) Oscillation-timing differences between responses to positive- and negative-polarity stimuli vs square pulse duration for the same receptors shown in G. (I, J) Extracellular recordings from an oscillating receptor in P. tenuicauda in response to a head-positive (‘normal polarity’) conspecific EOD waveform (black) and the reverse-polarity waveform (red) at an intensity of 316 nA (I) and 32 nA (J). Traces from five stimulus repetitions are superimposed. (K) Vector strength vs phase difference of oscillatory responses to opposite-polarity conspecific EODs in P. tenuicauda. Each point represents the mean of responses from six receptors. Vector strength was averaged across stimulus polarity within each receptor before averaging across receptors. Error bars represent S.E.M. Closed circles indicate phase resets that were significantly different for normal- vs reversed-polarity EODs (Hotelling test for paired circular data, F > Fcrit = 6.9, p < 0.05). The stimulus intensities that evoked significantly different phase resets for opposite polarity EODs were 56, 178, and 316 nA. Intensities of 100 nA and <56 nA did not result in significantly different phase resets. (L) Phase differences between responses to positive- and negative-polarity stimuli vs square pulse duration for oscillatory responses to monopolar square electric pulses.DOI:http://dx.doi.org/10.7554/eLife.08163.005
Mentions: To understand sensory encoding by these receptors, we recorded responses to focal stimulation with monopolar square pulses (Figure 3). We delivered both positive- and negative-polarity pulses to mimic the stimulation that receptors at different locations on the fish's body would experience during a natural global stimulus (Hopkins and Bass, 1981). As shown previously, spiking receptors responded with a single time-locked spike in response to inward current transients (Bennett, 1965), which occur at the onset of a positive-polarity pulse and at the offset of a negative-polarity pulse (Figure 3A,B). Spike probability depended on pulse duration (Figure 3C) but was high for stimulus durations within the range of total durations of conspecific EODs (horizontal bars in Figure 3C).10.7554/eLife.08163.005Figure 3.Spiking receptors encode pulse duration, whereas oscillating receptors do 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.