Neurophysiology goes wild: from exploring sensory coding in sound proof rooms to natural environments

Abstract

To perform adaptive behaviours, animals have to establish a representation of the physical "outside" world. How these representations are created by sensory systems is a central issue in sensory physiology. This review addresses the history of experimental approaches toward ideas about sensory coding, using the relatively simple auditory system of acoustic insects. I will discuss the empirical evidence in support of Barlow's "efficient coding hypothesis", which argues that the coding properties of neurons undergo specific adaptations that allow insects to detect biologically important acoustic stimuli. This hypothesis opposes the view that the sensory systems of receivers are biased as a result of their phylogeny, which finally determine whether a sound stimulus elicits a behavioural response. Acoustic signals are often transmitted over considerable distances in complex physical environments with high noise levels, resulting in degradation of the temporal pattern of stimuli, unpredictable attenuation, reduced signal-to-noise levels, and degradation of cues used for sound localisation. Thus, a more naturalistic view of sensory coding must be taken, since the signals as broadcast by signallers are rarely equivalent to the effective stimuli encoded by the sensory system of receivers. The consequences of the environmental conditions for sensory coding are discussed.

Keywords: Acoustic communication; Insects; Masking; Sensory coding; Transmission channel.

Fig. 1

The coding of acoustic events in the nocturnal tropical rainforest of Panama is studied by the author and his PhD-student Alexander Lang, using the “biological microphone approach”. The action potential activity of the omega neuron of a rainforest katydid was recorded with a portable recording unit (left) about 1 h after sunset. A bat detector (upper line) was placed next to the preparation, indicating the highly repetitive echolocation calls of a bat passing by. Note that the neuron fires bursts of APs in response to these calls, but also to other bat calls that are not detected by the bat detector (red bars), most likely due to the different directionality of the technical and biological receivers. Bursts of APs are also elicited by unknown sources and in response to a playback of a short conspecific call of the katydid (asterisk) (Lang, Teppner and Römer, unpublished)

Fig. 2

Representative section of 30 s of nocturnal background noise recording as sonogram and oscillogram, respectively (a, b). Filtering of this sound section with a filter function derived from the tuning curve of AN1 in Diatrypa sp. (c) reveals an amplitude modulation coinciding with the bursting activity of the AN1 neuron (d). Bursts were elicited by sound events in the narrow frequency band between 3.5 and 4.5 kHz, representing calling songs of several Diatrypa males at various distances from the preparation (arrow in a). Modified from Schmidt et al. (2011)

Fig. 3

a Peri-stimulus time histograms of AN1 activity in Gryllus bimaculatus in response to a model of the calling song broadcast at a rate of 3/s at various distances from the source in natural grassland typical for a field cricket. Note the “silent spot” at a distance of 6 m (arrow) with a response at threshold, but with substantial suprathreshold response at larger distances (from Zorn-Pauly and Römer, unpublished). b Simultaneous field recording of left and right AN1 activity (smaller APs; larger APs are from AN2 neuron) at a distance of 10 m from the sound source outdoors. The conspecific chirp (lower panel) was presented at a stimulus angle 30° of the longitudinal body axis for the ipsilateral AN1. Note the change of correct and incorrect directional information (contralateral AN1 with stronger activity, asterisks) over time at the same location. In addition to binaural discharge differences, binaural latency differences as potential cues for directional information were analysed. In most experiments, the latency differences closely correlated with the maxima and minima of discharge differences, but at some distances, latency differences were large, whereas the discharge differences approached zero. Time bar in A and B 350 ms. (Kostarakos and Römer unpublished)

Fig. 4

Responses of the likely homologue of AN2 in a rainforest cricket (Int-2; APs with smaller amplitude) to the bat echolocation call of Saccopteryx bilineata and to calls of two rainforest katydids (Anapolisia colossea and Ectemia dumicolaia). Note the similar responses with very high rates of APs to single, short sound pulses (Brunnhofer and Römer, unpublished)