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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.


Synchrony across receptors is greatest for the first poststimulus oscillation and then rapidly declines.(A) Responses of three oscillating receptors in P. tenuicauda to a single square pulse delivered in sequential recordings. Responses to each of 10 stimulus presentations are shown in gray and averages are shown in black, red, or blue. Dotted vertical lines in the corresponding color denote the times of the first four poststimulus oscillatory peaks. Yellow bars group the first, second, third, and fourth peaks from each receptor. Note how the peaks are transiently synchronized just after the stimulus, but become increasingly asynchronous with each subsequent cycle. (B) Same as A for responses of the same three receptors to a 3-ms IPI stimulus. Note the transient increase in synchrony across receptors just after both stimulus pulses. (C) A single recording trace from four receptors in the right augenrosette of one P. tenuicauda in response to a normal- (black) and reversed- (red) polarity conspecific EOD. Recording traces were normalized to the amplitude of the first poststimulus oscillation. (D) The sum of the normalized responses of all 36 receptors in the right augenrosette of one P. tenuicauda (illustrated in Figure 2B) to a normal- and reversed-polarity conspecific EOD (this includes the four traces shown in C as well as responses from the 32 additional receptors). The enhanced synchrony across receptors for the first poststimulus oscillatory peak results in the largest peak in the summed response just after the stimulus.DOI:http://dx.doi.org/10.7554/eLife.08163.008
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fig6: Synchrony across receptors is greatest for the first poststimulus oscillation and then rapidly declines.(A) Responses of three oscillating receptors in P. tenuicauda to a single square pulse delivered in sequential recordings. Responses to each of 10 stimulus presentations are shown in gray and averages are shown in black, red, or blue. Dotted vertical lines in the corresponding color denote the times of the first four poststimulus oscillatory peaks. Yellow bars group the first, second, third, and fourth peaks from each receptor. Note how the peaks are transiently synchronized just after the stimulus, but become increasingly asynchronous with each subsequent cycle. (B) Same as A for responses of the same three receptors to a 3-ms IPI stimulus. Note the transient increase in synchrony across receptors just after both stimulus pulses. (C) A single recording trace from four receptors in the right augenrosette of one P. tenuicauda in response to a normal- (black) and reversed- (red) polarity conspecific EOD. Recording traces were normalized to the amplitude of the first poststimulus oscillation. (D) The sum of the normalized responses of all 36 receptors in the right augenrosette of one P. tenuicauda (illustrated in Figure 2B) to a normal- and reversed-polarity conspecific EOD (this includes the four traces shown in C as well as responses from the 32 additional receptors). The enhanced synchrony across receptors for the first poststimulus oscillatory peak results in the largest peak in the summed response just after the stimulus.DOI:http://dx.doi.org/10.7554/eLife.08163.008

Mentions: Although interoscillation intervals accurately represent IPIs longer than ∼1 ms, how would the system disambiguate these stimulus-evoked oscillatory peaks from ongoing oscillations? Phase resets in oscillatory receptors serve to transiently synchronize the population in response to a stimulus (Figure 6). Because oscillation frequency varies across receptors, responses rapidly desynchronize (Figure 6). For instance, in response to a single square pulse, across-receptor synchrony is greatest for the first poststimulus oscillatory peak (Figure 6A). In response to a pair of pulses, across-receptor synchrony is high immediately following each pulse and rapidly decreases (Figure 6B). To further illustrate this, we recorded responses to a single conspecific EOD of normal and reversed polarities from all 36 receptors in a single rosette of one P. tenuicauda (same receptors illustrated in Figure 2B). Responses from four of these receptors are shown in Figure 6C. Notice that again, across-receptor synchrony is greatest for the first poststimulus oscillation, but then rapidly declines. Summing responses across all 36 receptors resulted in a single, distinct peak immediately following the stimulus (Figure 6D), due to a transient synchronization across receptors followed by increasing asynchrony of receptors oscillating at different frequencies. In this way, the electrosensory system could use synchrony across the population of receptors to distinguish between stimulus-evoked and spontaneous oscillation cycles.10.7554/eLife.08163.008Figure 6.Synchrony across receptors is greatest for the first poststimulus oscillation and then rapidly declines.


Peripheral sensory coding through oscillatory synchrony in weakly electric fish.

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

Synchrony across receptors is greatest for the first poststimulus oscillation and then rapidly declines.(A) Responses of three oscillating receptors in P. tenuicauda to a single square pulse delivered in sequential recordings. Responses to each of 10 stimulus presentations are shown in gray and averages are shown in black, red, or blue. Dotted vertical lines in the corresponding color denote the times of the first four poststimulus oscillatory peaks. Yellow bars group the first, second, third, and fourth peaks from each receptor. Note how the peaks are transiently synchronized just after the stimulus, but become increasingly asynchronous with each subsequent cycle. (B) Same as A for responses of the same three receptors to a 3-ms IPI stimulus. Note the transient increase in synchrony across receptors just after both stimulus pulses. (C) A single recording trace from four receptors in the right augenrosette of one P. tenuicauda in response to a normal- (black) and reversed- (red) polarity conspecific EOD. Recording traces were normalized to the amplitude of the first poststimulus oscillation. (D) The sum of the normalized responses of all 36 receptors in the right augenrosette of one P. tenuicauda (illustrated in Figure 2B) to a normal- and reversed-polarity conspecific EOD (this includes the four traces shown in C as well as responses from the 32 additional receptors). The enhanced synchrony across receptors for the first poststimulus oscillatory peak results in the largest peak in the summed response just after the stimulus.DOI:http://dx.doi.org/10.7554/eLife.08163.008
© Copyright Policy
Related In: Results  -  Collection

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

fig6: Synchrony across receptors is greatest for the first poststimulus oscillation and then rapidly declines.(A) Responses of three oscillating receptors in P. tenuicauda to a single square pulse delivered in sequential recordings. Responses to each of 10 stimulus presentations are shown in gray and averages are shown in black, red, or blue. Dotted vertical lines in the corresponding color denote the times of the first four poststimulus oscillatory peaks. Yellow bars group the first, second, third, and fourth peaks from each receptor. Note how the peaks are transiently synchronized just after the stimulus, but become increasingly asynchronous with each subsequent cycle. (B) Same as A for responses of the same three receptors to a 3-ms IPI stimulus. Note the transient increase in synchrony across receptors just after both stimulus pulses. (C) A single recording trace from four receptors in the right augenrosette of one P. tenuicauda in response to a normal- (black) and reversed- (red) polarity conspecific EOD. Recording traces were normalized to the amplitude of the first poststimulus oscillation. (D) The sum of the normalized responses of all 36 receptors in the right augenrosette of one P. tenuicauda (illustrated in Figure 2B) to a normal- and reversed-polarity conspecific EOD (this includes the four traces shown in C as well as responses from the 32 additional receptors). The enhanced synchrony across receptors for the first poststimulus oscillatory peak results in the largest peak in the summed response just after the stimulus.DOI:http://dx.doi.org/10.7554/eLife.08163.008
Mentions: Although interoscillation intervals accurately represent IPIs longer than ∼1 ms, how would the system disambiguate these stimulus-evoked oscillatory peaks from ongoing oscillations? Phase resets in oscillatory receptors serve to transiently synchronize the population in response to a stimulus (Figure 6). Because oscillation frequency varies across receptors, responses rapidly desynchronize (Figure 6). For instance, in response to a single square pulse, across-receptor synchrony is greatest for the first poststimulus oscillatory peak (Figure 6A). In response to a pair of pulses, across-receptor synchrony is high immediately following each pulse and rapidly decreases (Figure 6B). To further illustrate this, we recorded responses to a single conspecific EOD of normal and reversed polarities from all 36 receptors in a single rosette of one P. tenuicauda (same receptors illustrated in Figure 2B). Responses from four of these receptors are shown in Figure 6C. Notice that again, across-receptor synchrony is greatest for the first poststimulus oscillation, but then rapidly declines. Summing responses across all 36 receptors resulted in a single, distinct peak immediately following the stimulus (Figure 6D), due to a transient synchronization across receptors followed by increasing asynchrony of receptors oscillating at different frequencies. In this way, the electrosensory system could use synchrony across the population of receptors to distinguish between stimulus-evoked and spontaneous oscillation cycles.10.7554/eLife.08163.008Figure 6.Synchrony across receptors is greatest for the first poststimulus oscillation and then rapidly declines.

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.