Filtering of behaviourally relevant temporal parameters of a grasshopper's song by an auditory interneuron

Abstract

In females of the acridid grasshopperChorthippus biguttulus, thoracic auditory interneurons were investigated with respect to their selectivity for temporal parameters of the conspecific song. Special attention was given to the detection of small gaps in the 'syllables' of the song, since behavioural experiments have shown that the presence or absence of gaps is critical for the female's Innate Releasing Mechanism (cf. Fig. 1).The spiking response of one ascending interneuron, the AN4, shows filtering properties which closely resemble the behavioural reactions (cf. Figs. 1, 3 and 5b). The difference in the AN4's reaction to stimuli with gaps and uninterrupted stimuli is maintained over the behaviourally relevant intensity range (Fig. 4). This reaction is reliable enough that the stimulus type could be inferred by higher centres even from single stimulus presentations. Hence, this neuron is likely to participate in the task of gap detection and probably is a part of the neuronal filter network which determines the characteristics of the Innate Releasing Mechanism of this species. However, this interneuron is not species-specific: A homologue exists in other acridids as well and, in Locusta migratoria, has similar response characteristics (Fig. 6). The inferences of this observation for the evolution of an Innate Releasing Mechanism are discussed.

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

“…The ascending neuron AN4 is strongly inhibited by songs exhibiting such gaps. A strong cotuning between the firing rate of AN4 and the behavioral response has been shown before (31), indicating that this neuron explicitly encodes a male's quality. A third song parameter strongly influencing female choice is the onset slope of the song's subunits.…”

“…Note that we study responses of neurons of one species of acridid grasshoppers-Locusta migratoria-to courtship signals of another species-C. biguttulus. This is well-justified, as auditory neurons in the early stages of sensory processing are morphologically and physiologically highly similar (15,16,31).…”

“…Hence, the labeled-line code observed at the third neuronal layer is not explicitly derived from another labeled-line code, but has to be established de novo by a transformation of the stimulus representation in the first two layers. The construction of this labeled line from uniformly tuned inputs is presumably achieved by adaptation and a well-timed interplay of excitation and inhibition (30,31).…”

Nonlinear Computations Underlying Temporal and Population Sparseness in the Auditory System of the Grasshopper

“…To study the responses of the models to natural signals, we used a set of songs from eight different male grasshoppers of the species Chorthippus biguttulus (Clemens et al, 2011). It is well justified to use models fit to neurons recorded in one species of grasshopper, L. migratoria, to study the responses to signals of another species, C. biguttulus, as the morphological and physiological properties of neurons at the early stages of processing we are interested in are highly similar (Ronacher and Stumpner, 1988;Neuhofer et al, 2008, Creutzig et al, 2009. As the song's amplitude increases over its duration, we used the last 400 ms where the amplitude plateaued.…”

Auditory processing at two time scales by the cricketGryllus bimaculatus

“…However, at the level of pattern processing, there do not appear to be many examples for which such an inhibition of responses to unattractive features of a song pattern was described. A notable exception is gap detection in female grasshoppers (von Helversen and von Helversen, 1997;Ronacher and Stumpner, 1988). Recent reports about the receptive fields of visual interneurons showed that a broadly tuned inhibition serves to sharpen response profiles by changing the balance between excitation and inhibition (Xing et al, 2011;Isaacson and Scanziani, 2011).…”