Solutions to the cocktail party problem in insects: selective filters, spatial release from masking and gain control in tropical crickets

Abstract

Background: Insects often communicate by sound in mixed species choruses; like humans and many vertebrates in crowded social environments they thus have to solve cocktail-party-like problems in order to ensure successful communication with conspecifics. This is even more a problem in species-rich environments like tropical rainforests, where background noise levels of up to 60 dB SPL have been measured.

Principal findings: Using neurophysiological methods we investigated the effect of natural background noise (masker) on signal detection thresholds in two tropical cricket species Paroecanthus podagrosus and Diatrypa sp., both in the laboratory and outdoors. We identified three 'bottom-up' mechanisms which contribute to an excellent neuronal representation of conspecific signals despite the masking background. First, the sharply tuned frequency selectivity of the receiver reduces the amount of masking energy around the species-specific calling song frequency. Laboratory experiments yielded an average signal-to-noise ratio (SNR) of -8 dB, when masker and signal were broadcast from the same side. Secondly, displacing the masker by 180° from the signal improved SNRs by further 6 to 9 dB, a phenomenon known as spatial release from masking. Surprisingly, experiments carried out directly in the nocturnal rainforest yielded SNRs of about -23 dB compared with those in the laboratory with the same masker, where SNRs reached only -14.5 and -16 dB in both species. Finally, a neuronal gain control mechanism enhances the contrast between the responses to signals and the masker, by inhibition of neuronal activity in interstimulus intervals.

Conclusions: Thus, conventional speaker playbacks in the lab apparently do not properly reconstruct the masking noise situation in a spatially realistic manner, since under real world conditions multiple sound sources are spatially distributed in space. Our results also indicate that without knowledge of the receiver properties and the spatial release mechanisms the detrimental effect of noise may be strongly overestimated.

Figure 1. Conspecific stimuli and masker used for experiments.

(A) Oscillograms of calling songs of Diatrypa sp. and Paroecanthus podagrosus at two time scales. (B) Power spectral density of typical background noise recordings (M1, blue and M2, black) of the nighttime rainforest on BCI, Panama. An additional frequency band was digitally mixed with the M1 recording to account for low acoustic energy at frequencies between 3.4 and 4 kHz (M3, red dashed line). Recordings with these spectra were used as maskers in neurophysiological experiments.

Figure 2. A. Frequency tuning of the AN1 neuron in Diatrypa sp.

(N = 6). (B) Standardized mean frequency tuning (±SE), with the best frequency of individual tuning curves set at 0 kHz/0 dB and higher thresholds to lower and higher frequencies arranged accordingly.

Figure 3. Results of spatial release from masking experiments in the laboratory (P. podagrosus).

Comparison of SNRs at masked thresholds with masker M1/M2 (black squares; N = 12) and M3 (grey squares; N = 6) for ipsilateral (masker and signal presented from the same side of the recorded AN1) and contralateral masker position (masker spatially separated by 180°).

Figure 4. Comparison of SNRs at masked thresholds outdoors and in the laboratory.

(P. podagrosus lab N = 5, outdoor N = 6; Diatrypa sp. lab N = 1, outdoor N = 5). Note the difference in SNRs in the real world situation and laboratory, although the masker M2 recorded at the site where outdoor experiments were performed was very similar spectrally and with respect to average intensity (55 dB SPL).

Figure 5. Selective response of AN1 in Diatrypa sp. towards conspecific signals embedded in noise outdoors.

Sonogram (A) and oscillogram (B) of a 30 seconds section of nocturnal background noise recorded simultaneously with AN1 activity (D) in the natural habitat. (C) Amplitude modulation resulting from filtering the signal in (B) with the species-specific AN1 filter function of Diatrypa sp. (standardized tuning curve), revealing calling songs of various males at different distances from the preparation (see arrow in A). Note the high correlation between the RMS amplitude of the filtered noise (E) with the firing pattern of AN1 (F).

Figure 6. Signal representation in neuronal activity is enhanced by a gain control mechanism.

(A) Representative neuronal response of AN1 in P. podagrosus to conspecific calling songs under masking noise (SNR −6 dB). Note reduced action potential activity during interstimulus intervals (ISI) compared with the noise-alone situation. (B) Quantification of suppression of the response to noise for three different SNRs (N = 8). Grey bars show the average spike rate during ISI compared with noise-alone (black bar, control). The average stimulus intensity in all experiments was 54.4±1.2 dB SPL.