B. Ronacher

Single auditory neurons rapidly discriminate conspecific communication signals

Animals that rely on acoustic communication to find mates, such as grasshoppers, are astonishingly accurate in recognizing song patterns that are specific to their own species. This raises the question of whether they can also solve a far more complicated task that might provide a basis for mate preference and sexual selection: to distinguish individual songs by detecting slight variations around the common species-specific theme. Using spike-train discriminability to quantify the precision of neural responses from the auditory periphery of a model grasshopper species, we show that information sufficient to distinguish songs is readily available at the single-cell level when the spike trains are analyzed on a millisecond time scale.

Temperature dependence of temporal resolution in an insect nervous system

Abstract. The vast majority of animals are poikilotherms, and thus face the problem that the temperature of their nervous systems rather smoothly follows the temperature changes imposed by their environment. Since basic properties of nerve cells, e.g., the time constants of ion channels, strongly depend on temperature, a temperature shift likely affects the processing of the temporal structure of sensory stimuli. This can be critical in acoustic communication systems in which time patterns of signals are decisive for recognition by the receiver. We investigated the temperature dependence of the responses of locust auditory receptors and interneurons by varying the temperature of the experimental animals during intracellular recordings. The resolution of fast amplitude modulations of acoustic signals was determined in a gap detection paradigm. In auditory receptors and local (second order) interneurons, temporal resolution was improved at higher temperatures. This gain could be attributed to a higher precision of spike timing. In a third-order neuron, a rise in temperature affected the interactions of inhibition and excitation in a complex manner, also resulting in a better resolution of gaps in the millisecond range.

Variability of spike trains and the processing of temporal patterns of acoustic signals—problems, constraints, and solutions

Object recognition and classification by sensory pathways is rooted in spike trains provided by sensory neurons. Nervous systems had to evolve mechanisms to extract information about relevant object properties, and to separate these from spurious features. In this review, problems caused by spike train variability and counterstrategies are exemplified for the processing of acoustic signals in orthopteran insects. Due to size limitations of their nervous system we expect to find solutions that are stripped to the computational basics. A key feature of auditory systems is temporal resolution, which is likely limited by spike train variability. Basic strategies to reduce such variability are to integrate over time, or to average across several neurons. The first strategy is constrained by its possible interference with temporal resolution. Grasshoppers do not seem to explore temporal integration much, in spite of the repetitive structure of their songs, which invites for ‘multiple looks’ at the signal. The benefits of averaging across neurons depend on uncorrelated responses, a factor that may be crucial for the performance and evolution of small nervous systems. In spite of spike train variability the temporal information necessary for the recognition of conspecifics is preserved to a remarkable degree in the auditory pathway.

Coding of a sexually dimorphic song feature by auditory interneurons of grasshoppers: the role of leading inhibition.

Abstract. The shape of stimulus onset is a distinct feature of many acoustic communication signals. In some grasshopper species the steepness of amplitude rise of the pulses which comprise the song subunits is sexually dimorphic and a major criterion of sex recognition. Here, we describe potential mechanisms by which auditory interneurons could transmit the information on onset steepness from the metathoracic ganglion to the brain of the grasshopper. Since no single interneuron unequivocally encoded onset steepness, it appears that this information has to reside in the relative spike counts or the relative spike timing of a small group of ascending auditory interneurons. The decisive component of this mechanism seems to be the steepness-dependent leading inhibition displayed by two interneurons (AN3, AN4). The inhibition increased with increasing onset steepness, thus delayed the excitatory response, and in one interneuron even strongly reduced the spike count. Other ascending interneurons, whose responses were little affected by onset steepness, could serve as reference neurons (AN6, AN12). Thus, our results suggest that a comparison of both, spike count and first-spike timing within a small set of ascending interneurons could yield the information on signal onset steepness, that is on the sex of the sender.

Asymmetrical integration of sensory information during mating decisions in grasshoppers

Significance Decision-making involves integrating different pieces of sensory information over time. Looking at how sensory information is weighted and integrated during a natural behavior can yield insight into the evolutionary forces shaping that behavior. Here, we investigated how female grasshoppers of the species Chorthippus biguttulus integrate information provided by male calling songs. Fitting a drift-diffusion model to behavioral data, we find that integration is highly asymmetrical: an unattractive song subunit far outweighs an attractive subunit. This asymmetrical integration is consistent with theories of sexual selection because it helps females avoid potentially costly interactions with unsuitable mating partners if the song belongs to another species or indicates a low-quality male; moreover, it suggests that song-based decision-making in grasshoppers is optimized by evolution. Decision-making processes, like all traits of an organism, are shaped by evolution; they thus carry a signature of the selection pressures associated with choice behaviors. The way sexual communication signals are integrated during courtship likely reflects the costs and benefits associated with mate choice. Here, we study the evaluation of male song by females during acoustic courtship in grasshoppers. Using playback experiments and computational modeling we find that information of different valence (attractive vs. nonattractive) is weighted asymmetrically: while information associated with nonattractive features has large weight, attractive features add little to the decision to mate. Accordingly, nonattractive features effectively veto female responses. Because attractive features have so little weight, the model suggests that female responses are frequently driven by integration noise. Asymmetrical weighting of negative and positive information may reflect the fitness costs associated with mating with a nonattractive over an attractive singer, which are also highly asymmetrical. In addition, nonattractive cues tend to be more salient and therefore more reliable. Hence, information provided by them should be weighted more heavily. Our findings suggest that characterizing the integration of sensory information during a natural behavior has the potential to provide valuable insights into the selective pressures shaping decision-making during evolution.

Long Rise Times of Acoustic Stimuli Improve Directional Hearing in Grasshoppers

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Response recovery in the locust auditory pathway.

Temporal resolution and the time courses of recovery from acute adaptation of neurons in the auditory pathway of the grasshopper Locusta migratoria were investigated with a response recovery paradigm. We stimulated with a series of single click and click pair stimuli while performing intracellular recordings from neurons at three processing stages: receptors and first and second order interneurons. The response to the second click was expressed relative to the single click response. This allowed the uncovering of the basic temporal resolution in these neurons. The effect of adaptation increased with processing layer. While neurons in the auditory periphery displayed a steady response recovery after a short initial adaptation, many interneurons showed nonlinear effects: most prominent a long-lasting suppression of the response to the second click in a pair, as well as a gain in response if a click was preceded by a click a few milliseconds before. Our results reveal a distributed temporal filtering of input at an early auditory processing stage. This set of specified filters is very likely homologous across grasshopper species and thus forms the neurophysiological basis for extracting relevant information from a variety of different temporal signals. Interestingly, in terms of spike timing precision neurons at all three processing layers recovered very fast, within 20 ms. Spike waveform analysis of several neuron types did not sufficiently explain the response recovery profiles implemented in these neurons, indicating that temporal resolution in neurons located at several processing layers of the auditory pathway is not necessarily limited by the spike duration and refractory period.