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T-Cell Responses to Pure Tones 3227 The Journal of Experimental Biology 203, 3225–3242 (2000) 3225 Printed in Great Britain © The Company of Biologists Limited 2000 JEB2896 NEUROETHOLOGY OF THE KATYDID T-CELL I. TUNING AND RESPONSES TO PURE TONES PAUL A. FAURE*,‡ AND RONALD R. HOY Section of Neurobiology and Behavior, Cornell University, Seeley G. Mudd Hall, Ithaca, NY 14853-2702, USA *Present address: Department of Psychology, University of Washington, Guthrie Hall, Box 351525, Seattle, WA 98195-1525, USA ‡Author for correspondence (e-mail: [email protected]) Accepted 27 July; published on WWW 9 October 2000 Summary The tuning and pure-tone physiology of the T-cell which supports early T-cell research showing that prothoracic auditory interneuron were investigated in the excitation of the contralateral ear inhibits ipsilateral T- nocturnal katydid Neoconocephalus ensiger. The T-cell is cell responses. In a temporal summation experiment, the extremely sensitive and broadly tuned, particularly to integration time of the T-cell at 40 kHz (integration time high-frequency ultrasound (у20 kHz). Adult thresholds constant τ=6.1 ms) was less than half that measured at were lowest and showed their least variability for 15 kHz (τ=15.0 ms). Moreover, T-cell spiking in response frequencies ranging from 25 to 80 kHz. The average best to short-duration pure-tone trains mimicking calling threshold of the T-cell in N. ensiger ranged from 28 to conspecifics (15 kHz) and bat echolocation hunting 38 dB SPL and the best frequency from 20 to 27 kHz. In sequences (40 kHz) revealed that temporal pattern- females, the T-cell is slightly more sensitive to the range of copying was superior for ultrasonic stimulation. frequencies encompassing the spectrum of male song. Apparently, T-cell responses are reduced or inhibited by Tuning of the T-cell in non-volant nymphs was stimulation with audio frequencies, which leads to the comparable with that of adults, and this precocious prediction that the T-cell will encode conspecific song less ultrasound sensitivity supports the view that it has a role well than bat-like frequency-modulated sweeps during in the detection of terrestrial sources of predaceous acoustic playback. The fact that the T-cell is one of the ultrasound. In adults, T-cell tuning is narrower than that most sensitive ultrasound neurons in tympanate insects is of the whole auditory (tympanic) organ, but only at audio most consistent with it serving an alarm, warning or frequencies. Superthreshold physiological experiments escape function in both volant and non-volant katydids revealed that T-cell responses were ultrasound-biased, (nymphs and adults). with intensity/response functions steeper and spike latencies shorter at 20, 30 and 40 kHz than at 5, 10 and Key words: auditory physiology, bioacoustics, bushcricket, hearing, 15 kHz. The same was also true for T-cell stimulation at insect, Neoconocephalus ensiger, neurophysiology, Orthoptera, 90 ° compared with stimulation at 0 ° within a frequency, Tettigoniidae, ultrasound. Introduction The functions of sound production and hearing in phonotaxis). Given their small size, the problem of sound orthopteran insects (crickets, katydids, locusts and their localization by insects is not trivial and, not surprisingly, this allies) include territoriality and aggression, mate recognition, topic has been a central question in insect auditory research localization of conspecifics, courtship, defense and predator (e.g. Michelsen and Nocke, 1974; Lewis, 1992; Michelsen, detection (see Alexander, 1962, 1967; Huber et al., 1989; 1992, 1998; Römer, 1992; Michelsen et al., 1994a,b; Schul Bailey and Rentz, 1990). Because of the tremendous diversity et al., 1999). Indeed, the majority of research on the acoustic of sounds that are produced and the importance of these Orthoptera has focused on understanding the behavioral signals to their everyday lives (i.e. survival and and/or neural mechanisms underlying sound localization reproduction), considerable research effort has been devoted during positive phonotaxis (e.g. von Helversen, 1984; to understanding peripheral and central auditory processing Rheinlaender and Römer, 1980, 1986; Schildberger and in the acoustic Orthoptera. In most orthopterans, it is the male Hörner, 1988; Schildberger et al., 1988; Stumpner, 1997; that stridulates to produce the loud, long-range, species- Schul, 1998, 1999; Römer and Krusch, 2000), with specific advertisement signal (mate-calling song) to which considerably fewer studies devoted to the detection and sexually receptive females may be attracted (i.e. positive processing of other biologically relevant signals such as 3226 P. A. FAURE AND R. R. HOY sounds produced by predators (i.e. negative phonotaxis, but was later found to reside in the prothoracic ganglion (Fig. 1A; see reviews by Hoy et al., 1989; Hoy, 1992). Oldfield and Hill, 1983; Zhantiev and Korsunovskaja, 1983; The purpose of this study is to identify neural correlates Rheinlaender and Römer, 1986; Römer et al., 1988). of behavioral responses to non-social acoustic stimuli in a Aficionados of insect hearing will be interested to learn that nocturnal katydid, the eastern sword-bearer conehead the T-cell was originally named without reference to its T- Neoconocephalus ensiger Harris (Orthoptera: Tettigoniidae). shaped morphology: the T stands for tympanic organ; hence, When stimulated with pulsed ultrasound, tethered N. ensiger the large unit excited by acoustic stimulation was named the T momentarily cease flying and alter their flight course, large fiber (N. Suga, personal communication). Technically, presumably to avoid predation by aerially hawking the T-cell is only one member of a class of T-shaped echolocating bats (Libersat and Hoy, 1991). Similar interneurons (e.g. crickets, Atkins and Pollack, 1987; mole ultrasound-induced types of escape behavior, more generally crickets, Mason et al., 1998; haglids, Mason and Schildberger, referred to as acoustic startle responses, have been reported in 1993; katydids, Rheinlaender et al., 1972; Shen, 1993; Schul, a variety of nocturnal insects including moths (Roeder, 1962), 1997); however, to be consistent with the previous literature, crickets (Moiseff et al., 1978), lacewings (Miller and Olesen, we will refer to it as the T-cell. 1979), locusts (Robert, 1989), mantids (Yager et al., 1990) and Previous authors have suggested that katydid acoustic beetles (Forrest et al., 1995; Yager and Spangler, 1997). startle responses may be mediated by the pair of prothoracic Recently, we have shown that N. ensiger possess a second, T-cell auditory interneurons (e.g. McKay, 1969, 1970). Römer previously unknown, type of acoustic startle response: et al. (1988) found that the onset of synaptic activity in cessation of singing (Faure and Hoy, 2000a). When stimulated the T-cell was delayed by only 0.8–1.2 ms relative to with pulsed ultrasound, stridulating males cease calling and primary receptors located micrometers away, implying a may remain motionless (and cryptic), drop and/or jump to the monosynaptic connection. Such fast throughput is consistent ground, where they hide by burrowing into the vegetation, or with the T-cell functioning in a predator-detection circuit, but take to the wing (evasive flight). As with cessation of flight, other physiological data are inconclusive in assigning a role cessation of song (i.e. silencing oneself) presumably evolved to the katydid T-cell. Various aspects of T-cell physiology as a way of avoiding predators, in this case acoustically have been investigated, including lesion and contralateral orienting predators such as cats, mice, shrews and substrate- inhibition studies (Suga and Katsuki, 1961a; McKay, gleaning bats (Walker, 1964; Sales and Pye, 1974; Belwood 1969, 1970; Rheinlaender et al., 1972), the effects of and Morris, 1987). pharmacological agents (Suga and Katsuki, 1961b), encoding Threshold tuning curves for the two acoustic startle of directional acoustic stimuli (Suga, 1963; Rheinlaender et responses are virtually identical, suggesting that a common al., 1972, 1986; Rheinlaender and Römer, 1980), responses to neural mechanism underlies both forms of escape (Faure and conspecific and/or heterospecific katydid song (Suga and Hoy, 2000a). For such a mechanism to function adequately, Katsuki, 1961a; Kalmring et al., 1979; Zhantiev and however, it must reliably distinguish conspecific song, which Korsunovskaja, 1983; Schul, 1997) and the use of the T-cell is broadband and contains both audio and ultrasonic as a ‘biological microphone’ (Rheinlaender and Römer, frequencies, from predatory ultrasound. Despite considerable 1986), but there have been few systematic studies of its overlap in the spectral and temporal characteristics of these basic response properties (but see Rheinlaender et al., 1972; signal categories, N. ensiger rarely show startle responses Rheinlaender, 1975). This is surprising considering how easy when listening to conspecific song but do so reliably when it is to identify and record from the T-cell using simple stimulated with bat-like ultrasound (Libersat and Hoy, 1991; extracellular techniques (e.g. Rheinlaender and Römer, 1986). Faure and Hoy, 2000a). Thus, our goal was to discover Moreover, none of the above studies has examined T-cell neurophysiological correlates underlying behavioral responses specifically in relation to predator detection. perception and sound categorization (Wyttenbach et al., 1996). In this paper, the first of a pair dealing with the physiology Within the acoustic Orthoptera, the presence
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