Marsat and Pollack Bursting and ultrasound avoidance model with 15 kHz carrier frequency typically elicited bipha- sic responses, in which initial steering away from the sound was replaced after a few seconds by steering toward the sound, suggesting inhibitory interactions between song-recognition and predator-avoidance systems (Pollack et al., 1984). Auditory information is processed initially by bilaterally paired, identiﬁed interneurons that receive monaural excitatory inputs from receptors (Hennig, 1988; Hardt and Watson, 1994). Two well studied and particularly important bilaterally paired neurons for the processing of ultrasound are Ascending Neuron 2 (AN2) and Omega Neuron 1 (ON1; Figure 2). AN2 is the main conduit by which information about ultrasound reaches the brain, and can thus be seen as a bottleneck in the ultrasound processing pathway. ON1 is a local interneuron; it receives input from the receptors of one ear and provides contralateral inhibition to several interneu- rons that receive input from the other ear, including AN2 and the contralateral ON1 (Selverston et al., 1985), thereby enhancing bilateral differences used to localize sound. Several high-frequency-sensitive brain neurons have been described, some of which, based on their anatomical and phys- iological characteristics, are candidates for receiving input directly from AN2 (Boyan, 1980, 1981; Schildberger, 1984; Brodfuehrer and Hoy, 1990); however paired simultaneous recordings from AN2 and its potential targets have not yet been performed. Such experiments are necessary not only to conﬁrm putative connec- tivity, but also to study the effects of AN2 bursts on its targets. One type of local brain neuron, which arborizes on both sides of the brain, is excited by ipsilateral sound pulses and inhibited by contralateral pulses and thus could, in principle, act as a bilat- eral comparator. Such a bilateral comparison could be involved in processing the spatial information of the sound necessary to direct behavior away from the source but nothing is known about this process. Another group of brain neurons, which are probably at least two synapses removed from AN2, carry the output of brain cir- cuits to lower ganglia where motor responses are generated (Boyan and Williams, 1981; Brodfuhrer and Hoy, 1989; Staudacher, 2001). The most interesting of these, with respect to avoidance responses, is a subset the activity of which is modulated by ﬂight (Brodfuhrer and Hoy, 1989). Negative phonotaxis to ultrasound occurs only when crickets are actively ﬂying (or, much more weakly, while walking: Pollack et al., 1984); quiescent animals do not respond to ultrasound, no matter how intense the stimulus. Thus, infor- mation about the sound stimulus and about behavioral state must be integrated somewhere along the processing chain. Flight has no effect on responses of AN2, ruling out early processing as the locus of this integration, but responses of several descending brain neurons are both stronger and more rapid during ﬂight than while animals are quiescent, pointing to the brain as the site where audi- tory and behavioral-state information are combined. Although responses are enhanced during ﬂight, the neurons do respond even while the animal is quiescent. Indeed, response magnitude of quiescent animals to intense stimuli can be larger than that of ﬂying animals to stimuli that, though less intense, are nevertheless above typical threshold for eliciting negative phonotaxis. Thus, the role of these descending neurons in triggering or controlling ﬂight-steering responses remains unclear. Nevertheless, key elements of the network generating the ultra- sound avoidance behavior are understood. AN2 in particular has a deterministic role in triggering avoidance steering even though it is on the sensory side of the pathway. The causal rela- tionship between AN2’s activity and avoidance steering was ﬁrst demonstrated by Nolen and Hoy (1984, 1986). They performed intracellular recording of AN2 in a tethered cricket while also mon- itoring the activity of muscles used for steering during ﬂight (see Figure 3). They showed that hyperpolarizing AN2 abolished the motor response to ultrasound, and that depolarizing AN2 evoked a motor response even though no sound was presented, thereby demonstrating AN2’s necessity and sufﬁciency. Thus, an interneu- ron directly post-synaptic to sensory receptors is the decisive trigger for ultrasound avoidance. Most interestingly, one prop- erty of AN2 underlies the decision to trigger avoidance steering or not: bursting. The temporal coding properties of AN2 were investigated by Marsat and Pollack (2005, 2006, 2007, 2010) using ultrasound stimuli with random amplitude modulations (Figure 1A), rather than using more naturalistic pulsed stimuli. The use of a “white noise” amplitude envelope is convenient because it allows one to quickly characterize the temporal tuning properties of the cell, and also reveals some of the coding strategies. Two key ﬁndings came from comparing the input – the pattern of amplitude modulation to be encoded – to the output spike train. First, AN2 is able to encode a wide range of amplitude modulation rates that encom- pass those typical of bat echolocation signals (Marsat and Pollack, 2005). Second, the neuron encodes the signal in a non-linear manner. Indeed, the input stimulus has a Gaussian amplitude dis- tribution but the output spike train has a bimodal distribution of ISI; the short ISIs of spikes within bursts form the ﬁrst peak in the distribution, and the longer ISIs between isolated spikes, or between bursts, form the second, broader, peak (Figure 1). Because ISI is the inverse of instantaneous ﬁring rate, the distrib- ution of the latter is also bimodal. No linear transformation can turn a Gaussian distribution signal into a bimodal distribution, and information-theoretic quantiﬁcation of AN2’s coding of stim- uli with white noise amplitude envelopes showed that the majority of the information is encoded non-linearly (Marsat and Pollack, 2005). Similar to bursting neurons in other sensory systems, AN2 bursts act as feature detectors (Marsat and Pollack, 2006), signal- ing the occurrence of speciﬁc patterns of amplitude modulation. Speciﬁcally, AN2 bursts are triggered by peaks in amplitude larger than the standard deviation of the stimulus, in other words, salient peaks in amplitude (Figure 1A). Bursts are very reliable in their timing and thus carry accurate information about the occurrence of these features. These response characteristics presumably allow differentiating background noise from those peaks in ultrasound amplitude that are most likely to originate from a hunting bat. The bursting characteristics of AN2 have a direct impact on behavior. Nolen and Hoy (1984, 1986) showed that AN2 evokes avoidance steering only if it ﬁres at 180 spikes/s or more. This threshold corresponds to the longest ISIs that occur in AN2’s bursts (s6 ms; Figure 1; Marsat and Pollack, 2005, 2006). Marsat and Pollack examined explicitly the relationships between bursts or isolated spikes and behavior (see Figure 3). They showed that avoidance steering was triggered only by bursts whereas spikes that Frontiers in Neuroscience | Decision Neuroscience July 2012 | Volume 6 | Article 95 | 4