763 Who, what, where? Recognition and localization of acoustic signals by insects Gerald Pollack Insects, like all hearing animals, must analyze acoustic signals Figure 1 to determine both their content and their location. Neurophysiological experiments, together with behavioral tests, are beginning to reveal the mechanisms underlying these signal-analysis tasks. Work summarized here focusses on two Gryllodinus odicus Uv. issues: first, how insects analyze the temporal structure of a single signal in the presence of other competing signals; and second, how the signal's location is represented by the Pteronemobius heydeni Fish. binaural difference in neural activity. Addresses Tartarogryllus bucharicus B.-B. Department of Biology, McGill University, 1205 Avenue Dr Penfield, Montreal, Quebec H3A 1B1, Canada; e-mail: [email protected] Tartarogryllus tartarus obscurior Uv. Current Opinion in Neurobiology 2000, 10:763–767 0959-4388/00/$ — see front matter Tartarogryllus burdigalensis Latr. © 2000 Elsevier Science Ltd. All rights reserved. Introduction The questions posed in the title refer to some of the core Oecanthus pellucens Scop. issues in animal communication. The recipients of a sen- sory signal need to know who produced the signal, what the signal’s content is, and where the signal originated. Sound, Gryllus campestris L. being both long-range and information-dense, is an excel- lent medium for communication. The information content of the signal is represented by structural features of the Gryllus bimaculatus Degeer sound such as its spectrum and pattern of amplitude mod- ulation. The recipient’s analysis of the message’s content (who? what?) and of its location (where?) must be done in Modicogryllus pallipalpis Farb. real time, often when several signals arrive simultaneously from different sources. These are daunting computational tasks, and understanding how they are performed by ner- Gryllus truncatus Farb. 0.2 s vous systems is a challenge for neurobiology. Current Opinion in Neurobiology Acoustic signaling is widespread among vertebrates but, The diversity of temporal patterns of cricket songs. The songs among invertebrates, hearing and acoustic communication illustrated are those of several European and Asian species. From [8]. are well developed only in insects, in which they serve behavioral functions such as detection of predators, loca- tion of mates, and location of hosts (for reviews, see [1–3]). rare exception [6], lack the ‘melodies’ that characterize Insects offer several advantages as model systems for neu- many vertebrate communication signals. The ears of many roethological studies, including robust behavior, easily insects are capable of spectral analysis, and there are sever- accessible nervous systems, and uniquely identifiable neu- al examples in which a signal’s spectrum may be rons that permit one to frame general questions about the informative (see [2,7] for reviews), but in most instances the neural analysis of signals at the levels both of single nerve main information-carrier in an insect’s song is its temporal cells and of the circuits they form [4,5]. In this review, I structure — in other words, the durations and shapes of will discuss some recent behavioral and neurophysiological sound pulses, the spacing between them, and their organi- experiments carried out on insects that are directed at the zation into higher-order groupings (Figure 1; [8]). problems of signal recognition and localization. Behavioral experiments, using synthetic song models, have outlined the properties of the temporal-pattern filters that Temporal pattern as a carrier of information analyze the signals; however, the neuronal implementation Insect songs generally consist of rhythmic sequences of of these filters is understood only in broad outline. more-or-less similar brief sounds (sound pulses), and, with Temporal-pattern filtering is mainly a central phenomenon; 764 Neurobiology of behaviour Figure 2 Figure 2 Selective attention to a single signal among many. S1, S2 and S3 represent three singers at different distances from the receiver, R. Because of the differences in distance, their songs arrive at R at different intensities, as illustrated in the oscillograms. The trace labeled S1 S1–3 shows what a microphone at the position of the receiver would detect (i.e. the summation of the three signals). The bottom trace represents the membrane potential of an interneuron, such as those described in [15,16,17•], that receives both fast-acting excitation and slow inhibition. Inhibition has lowered the neuron’s baseline membrane potential below its resting level (resting membrane potential, rmp; S2 represented by the arrow), with the result that only the largest sound- evoked excitatory postsynaptic potentials, produced by the loudest sound pulses, are sufficient to bring the membrane potential above threshold (dotted line). As a result, S1 and S2 are filtered out of the neuron’s spiking response. The anatomical relationships and relative response laten- cies of the different types of filter neurons suggest that band-pass selectivity is synthesized by combining inputs S3 from lower-level low- and high-pass filters [9]. Recent work suggests that even receptor neurons may, in some instances, play a role in temporal-pattern filtering. Many insect songs consist of long sequences of rapidly repeated sound pulses. Such stimuli induce sensory habituation — a decline in R responses to successive sound pulses within the sequence. The higher the pulse rate, the more pronounced the habit- uation; consequently, the receptor neurons act as low-pass temporal filters [10••]. This mechanism can only operate in species with songs that are conducive to habituation — long S1 sequences of rapidly repeated pulses. Such songs are, how- ever, common. Despite these basic low-pass filter S2 properties of the receptor neurons, the general conclusion, that strong temporal-pattern selectivity paralleling the selectivity of behavioral responses emerges only at higher S3 levels of neural circuitry, remains essentially correct. Providing high-quality input to the temporal- pattern filters S1–3 Insects often sing in aggregations [11–13] in which a lis- tener may be within earshot of several singers. In some species, individual signalers may avoid mutual interfer- ence by singing either in alternation or in synchrony with others [12], but in other species the listener is faced with the problem of teasing a single signal out of apparent Threshold cacophony (the ‘cocktail party’ problem). Crickets and rmp katydids solve this problem with a form of selective atten- tion [14–16,17•]. Some of their low-order auditory Current Opinion in Neurobiology interneurons receive mixed excitatory and inhibitory input. The excitation has a rapid time course, allowing the receptor neurons and low-order interneurons generally neurons to respond crisply and accurately to the pattern of copy the temporal pattern of the stimulus with high fideli- amplitude modulation. The inhibition, which is due in part ty. At higher levels, interneurons are found that respond to a Ca2+-activated current [18] (most probably, a K+ cur- most strongly only to particular stimulus temporal patterns. rent) is more leisurely, building up and, after the stimulus In the cricket Gryllus bimaculatus, for example, the first indi- has terminated, decaying over a period of several seconds. cation of temporal filtering is in brain neurons that are two The inhibition serves to down-regulate the neuron’s sensi- to three synapses removed from receptors. These neurons tivity such that signals of lower intensity are filtered out. show low-, high- or band-pass filter properties. The band- As a result, the temporal pattern of the most intense signal, pass-filter neurons respond best to the same range of corresponding to the loudest (or nearest) singer, remains temporal patterns that best evoke behavioral responses. relatively uncontaminated (Figure 2); thus a ‘clean’ copy of Recognition and localization of acoustic signals by insects Pollack 765 the signal can be passed on to the higher-level filter Figure 3 circuits for further processing. This same mechanism explains the remarkable ability of 1.0 t=0s these insects to discriminate reliably between simultaneous t=10s signals originating on the two sides [14,15,17•,19], a situa- 0.8 Ipsilateral tion that they presumably encounter frequently in the field. Each of the stimuli, when presented by itself, is detectable Contralateral by both ears, and so one might suppose that the simultane- 0.6 ous presence of many stimuli would result in their Relative response obscuring each other’s temporal pattern. However, sound 0.4 intensity at the two ears will differ, depending on the direc- tion of the sound source [20]. This auditory directionality, together with the slow inhibition described above, enables 0 10 20 30 (s) neurons on each side of the nervous system to ‘listen’ selec- Current Opinion in Neurobiology tively to the sound played on their side. The result is that distinct copies of the two songs can coexist in the nervous Intensity-dependent habituation may reverse the sign of the binaural system, one on each side. Presumably, these can then be difference in response strength. The inset shows a recording from the analyzed by recognizer circuits, also situated separately on auditory nerve of a cricket to a high-repetition-rate, high-intensity sequence of sound pulses (bottom trace). The top trace shows each side of the nervous system, with the behavioral out- responses immediately after onset of stimulation, and the second trace come (preference for one or the other of the songs) after 10 s of stimulation have elapsed. Responses to successive sound determined by comparing the outputs of the recognizers; pulses are quantified in the graph by integrating the nerve recording the side receiving the ‘best’ signal pattern wins [14,21]. over an appropriate time window surrounding each sound pulse. The points show responses of a single nerve to stimuli played from the ipsilateral and contralateral sides; this approximates the responses of The code for sound direction the two ears to a single stimulus played from one side.