Evolutionarily conserved coding properties of auditory neurons across grasshopper species

Neuhofer, Daniela; Wohlgemuth, Sandra; Stumpner, Andreas; Ronacher, Bernhard

doi:10.1098/rspb.2008.0527

Cited by 36 publications

(30 citation statements)

References 55 publications

(82 reference statements)

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“…1C,D). Its anatomical and stimulus-response characteristics are almost identical in different grasshopper species Neuhofer et al, 2008), indicating a highly conserved functional role. For the first part of our study, we recorded from C. biguttulus (n ϭ 3) and L. migratoria (n ϭ 3), as described in Materials and Methods.…”

Section: Resultsmentioning

confidence: 81%

Timescale-Invariant Representation of Acoustic Communication Signals by a Bursting Neuron

Creutzig

Wohlgemuth²,

Stumpner³

et al. 2009

J. Neurosci.

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Acoustic communication often involves complex sound motifs in which the relative durations of individual elements, but not their absolute durations, convey meaning. Decoding such signals requires an explicit or implicit calculation of the ratios between time intervals. Using grasshopper communication as a model, we demonstrate how this seemingly difficult computation can be solved in real time by a small set of auditory neurons. One of these cells, an ascending interneuron, generates bursts of action potentials in response to the rhythmic syllable-pause structure of grasshopper calls. Our data show that these bursts are preferentially triggered at syllable onset; the number of spikes within the burst is linearly correlated with the duration of the preceding pause. Integrating the number of spikes over a fixed time window therefore leads to a total spike count that reflects the characteristic syllable-to-pause ratio of the species while being invariant to playing back the call faster or slower. Such a timescale-invariant recognition is essential under natural conditions, because grasshoppers do not thermoregulate; the call of a sender sitting in the shade will be slower than that of a grasshopper in the sun. Our results show that timescale-invariant stimulus recognition can be implemented at the single-cell level without directly calculating the ratio between pulse and interpulse durations.

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Section: Resultsmentioning

confidence: 81%

Timescale-Invariant Representation of Acoustic Communication Signals by a Bursting Neuron

Creutzig

Wohlgemuth²,

Stumpner³

et al. 2009

J. Neurosci.

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“…Interestingly, the structure of the auditory network seems to be older than that of many songs it processes (15). It might thus be optimal for the songs but it is certainly not optimized for them.…”

Section: Discussionmentioning

confidence: 99%

“…Auditory stimuli consisted of eight songs from representative male individuals of the species Chorthippus biguttulus, whose auditory system is highly homologous to that of locusts at the stages considered here (13,15,16). Song recognition in these animals is based on the signal's envelope.…”

Section: Resultsmentioning

confidence: 99%

Efficient transformation of an auditory population code in a small sensory system

Clemens

Kutzki

Ronacher

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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Optimal coding principles are implemented in many large sensory systems. They include the systematic transformation of external stimuli into a sparse and decorrelated neuronal representation, enabling a flexible readout of stimulus properties. Are these principles also applicable to size-constrained systems, which have to rely on a limited number of neurons and may only have to fulfill specific and restricted tasks? We studied this question in an insect system-the early auditory pathway of grasshoppers. Grasshoppers use genetically fixed songs to recognize mates. The first steps of neural processing of songs take place in a small three-layer feedforward network comprising only a few dozen neurons. We analyzed the transformation of the neural code within this network. Indeed, grasshoppers create a decorrelated and sparse representation, in accordance with optimal coding theory. Whereas the neuronal input layer is best read out as a summed population, a labeled-line population code for temporal features of the song is established after only two processing steps. At this stage, information about song identity is maximal for a population decoder that preserves neuronal identity. We conclude that optimal coding principles do apply to the early auditory system of the grasshopper, despite its size constraints. The inputs, however, are not encoded in a systematic, map-like fashion as in many larger sensory systems. Already at its periphery, part of the grasshopper auditory system seems to focus on behaviorally relevant features, and is in this property more reminiscent of higher sensory areas in vertebrates.metric | invertebrates | information theory T o increase their fitness, most animals strive to evaluate sensory signals that reveal the quality of a potential mate. What if an animal has only a few dozen neurons to preprocess this extremely important information? Optimal coding theory suggests that the creation of a sparse, decorrelated representation would be a wise investment of scarce neuronal resources (1).That is indeed what has been found in many sensory modalities and species under natural conditions (2-4).These early sensory networks often comprise large numbers of cells and organize information in a map-like fashion, where spatial proximity of neurons reflects similarity in the selectivity for fundamental stimulus features (5, 6). These maps tend to have a complete representation of sensory space and enable subsequent processing steps to select relevant features based on attention or associative learning. Reading out such a representation by "blind" summation of responses across different neurons would be highly inefficient to recover information, because stimulus features are not only encoded by neuronal activity per se but also by neuronal identity. This type of population code is referred to as labeled-line code (7,8). Accordingly, higher-order sensory areas need to take into account which neurons are active when producing more specific representations of behaviorally relevant stimulus aspects (9). Do the...

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“…The parameters determining song integration during courtship likely reflect the costs and benefits associated with mate choice, and this is true even though the evolutionary optimization of decision-making during courtship is likely constrained in several ways. For instance, song evaluation in grasshoppers is shaped by selective pressures exerted on the auditory system by demands not directly associated with mate selection, such as the detection of predators (35). Also, traits that have evolved in contexts other than mate choice can induce perceptual biases that affect female decisions (5,6,36).…”

Section: Discussionmentioning

confidence: 99%

Asymmetrical integration of sensory information during mating decisions in grasshoppers

Clemens

Krämer

Ronacher

2014

Proc. Natl. Acad. Sci. U.S.A.

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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.O ne crucial decision in the lifetime of an animal is the decision with whom to mate. The males of many animals have evolved elaborate traits to attract females (1). These traits often involve the production of calling or courtship songs (2-4). Females base their decision to engage in courtship and to mate on the properties of these signals. Though many different factors drive and constrain the evolution of behavioral decisions in general (5, 6), the way information is integrated in the context of mate selection may reflect the fitness costs and benefits associated with mate choice. These costs depend on the mating system, e.g., the abundance of potential mating partners, the likelihood and costs of multiple matings, direct benefits of mating, and the costs of assessing a potential mate (7-10).Here, we investigate the implementation of a decision-making strategy by studying the integration of song features during courtship in grasshoppers. Acoustic courtship in the species Chorthippus biguttulus involves bidirectional communication. Males produce calling songs consisting of a sequence of simple stereotyped subunits-30-50 syllable-pause pairs. The female waits until the end of this song and indicates her readiness to further engage in a courtship ritual by producing a response song that allows the male to localize and approach the female (11) (Fig. 1A). This phase of courtship constitutes a first, important preselection step before females make their final assessment of an approaching mating partner. Not responding or responding to a male calling from a distance i...

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Evolutionarily conserved coding properties of auditory neurons across grasshopper species

Cited by 36 publications

References 55 publications

Timescale-Invariant Representation of Acoustic Communication Signals by a Bursting Neuron

Timescale-Invariant Representation of Acoustic Communication Signals by a Bursting Neuron

Efficient transformation of an auditory population code in a small sensory system

Asymmetrical integration of sensory information during mating decisions in grasshoppers

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