Gordon Atkins

Changes in phonotaxis by the female cricketAcheta domesticus L. after killing identified acoustic interneurons

SummaryPhonotactic selectivity of female crickets to natural and model calling songs (CSs) has been well documented. No identified acoustic interneurons or groups of them exhibited sufficiently selective responses to CSs to explain this behavioral selectivity. In this study identified acoustic interneurons were killed and pre- and post-killing phonotactic responses to model CSs were compared.1.Acoustic interneurons were iontophoretically filled with lucifer yellow. Surface illumination of the prothoracic ganglion with blue light (450 nm) stopped all EPSP and spiking activity and eliminated the membrane potential (Fig. 1).2.Control females oriented normally to a CS after immobilizing, exposing the prothoracic ganglion, recording intracellularly, and killing an acoustic unit not related to phonotaxis (Fig. 3).3.Killing one ON1 neuron resulted in an error angle when the female oriented to CSs with various syllable periods (SPs). However, direct orientation remained over a narrowed range of SPs, which were typical of an ‘ideal’ conspecific call (Figs. 4 and 5A). Elimination of both ON1s did not affect post-killing phonotaxis suggesting that the ON1 is not necessary for CS localization or recognition (Fig. 5B).4.Killing one ON2 resulted in angular errors similar to those following unilateral elimination of the ON1, but only in response to post-test CS SPs that were most attractive in pre-tests. Good posttest phonotaxis occurred to CSs with SPs found to be only marginally attractive in pre-tests (Fig. 6).5.Unilateral killing of AN2-type units produced post-test angular errors in orientation to all CS SPs. Presence of circling varied from animal to animal but if present occurred to all SPs (Fig. 7).

Regulation of cricket phonotaxis through hormonal control of the threshold of an identified auditory neuron.

Summary1.The phonotactic threshold of 3 to 5-day-old adult female Acheta domesticus and the threshold of the L1 auditory neuron drop progressively (Fig. 1).2.Application of juvenile hormone III (JHIII) to 1 -day-old females caused both the females threshold for phonotaxis and the threshold of the L1 auditory neuron to drop 20 or more dB over the next 12 h (Figs. 3, 4).3.JHIIFs effect on phonotactic threshold could be blocked by injection with a transcription (α-amanitin) or a translation blocker (emetine, Fig. 3).4.Injection of emetine also prevented the JHIII induced drop in L1s threshold (Fig. 4).5.Application of JHIII to the surface of, or microinjection of JHIII into one prothoracic hemiganglion caused the female to circle phonotactically away from the side of hormone addition at thresholds 25 to 35 dB lower than the pre-JHIII addition threshold within 2 h (Fig. 6).6.Application of JHIII to the surface of both prothoracic hemiganglia, accompanied by microinjection of emetine into one hemiganglion resulted in the female circling phonotactically toward the side receiving emetine injection, with a 25 to 35 dB drop in threshold (Fig. 6).

Evaluation of the behavioral roles of ascending auditory interneurons in calling song phonotaxis by the female cricket (Acheta domesticus)

Summary1.Inactivating one L1 results in angular errors and circling during orientation toward the side having the intact L1 in response to calling songs (CSs) whose intensities are below the threshold for L3 (Figs. 2, 3A). When song intensities are increased above the threshold of L3, circling decreases (Fig. 3B).2.Following inactivation of one L1 and occlusion of the ear providing input to the intact L1, no phonotaxis occurs in response to CSs at 60 dB (below the threshold of L3; Fig. 4A) demonstrating the necessity of L1 for phonotaxis. Orientation, at large and consistent angular errors (Fig. 5A) and circling (Fig. 5B) to the unoccluded side resumes when song intensities are increased above the threshold of L3 (Fig. 4B) suggesting that a single L3 can induce phonotactic responses.3.Inactivation of one L3 causes angular errors in orientation when CSs are above its threshold (Figs. 6A, 7), which are not apparent when CSs are below L3s threshold (Figs. 6B, 7).4.Inactivation of one L3 and occlusion of the ear providing input to the contralateral L1 and L3, leave only one L1 functioning. This results in turning and circling toward the unoccluded side containing the one functioning L1 (Figs. 6C, 8), thus confirming the sufficiency of L1 for phono taxis.

Age-correlated changes and juvenile hormone III regulation of the syllable period specific responses of the L3 auditory interneurons in the cricket, Acheta domesticus

Summary1.L3 is an auditory interneuron in the prothoracic ganglion of the cricket, Acheta domesticus. The degree of syllable period (SP) specific decrement to model calling songs is age-specific in L3. In response to calling songs having 50 ms SPs, L3s in old females (23–28 days) exhibit less response decrement than those in young (4 days) females (Figs. 1, 2).2.Two to 4 days after juvenile hormone III (JHIII) application to old females, L3s respond in a decrementing manner similar to those of young females. The changes in the SP selectivity of L3 by age and JHIII application, correlate well with changes that have been demonstrated to occur in the selectivity of phonotaxis under similar conditions (Fig. 3).3.The threshold of L3 does not change with age, while changes in L3s decrement result from decreased excitation in old females in response to the first syllable of a chirp (Figs. 4, 5).4.Injection of patterned current pulses (which reproduce the temporal pattern of the calling song) do not elicit decrement (Fig. 6).5.Age-related changes in selectivity to SP of the calling song occurs above and below L3s threshold (Fig. 7).

Influence of syllable period on song encoding properties of an ascending auditory interneuron in the cricketAcheta domestica

Summary1.L3 is a prothoracic auditory interneuron which has an ascending axon projecting to the brain. It is rather broadly tuned and most sensitive to carrier frequencies around 16 kHz (mean threshold=60 dB) and at 4–5 kHz (mean threshold=70 dB, Fig. 1).2.During open field stimulation L3s excitatory response increases rather linearly as sound intensity is increased and is 10–15 dB more sensitive to ipsilateral stimulation (Fig. 2). With closed field stimulation L3 is 45 dB more sensitive to ipsilateral sound at 16 kHz, and at least 20 dB more sensitive at 5 kHz (Fig. 3). With closed field sound, contralateral stimulation at subthreshold intensities (5 and 16 kHz) usually results in hyperpolarization (Fig. 3).3.L3s excitatory response to 16 kHz on the ipsilateral side is suppressed by low frequencies on the same side and by low and high frequency sounds from the contralateral side (Fig. 4).4.In open and closed field conditions, the number of spikes/syllable decrements in response to successive syllables of each chirp (Fig. 5). This response is dependent on the syllable period (SP) of the song, with the greatest decrement occurring in response to SPs of 50–70 ms; longer and shorter SPs cause less decrement (Figs. 6–7). At both 5 kHz and 16 kHz the ability of L3 to encode syllables (standard SD = 23 ms) within a chirp is dependent on the SP. At short SPs L3 fires throughout the chirp, while at longer SPs (50–200 ms) L3 responds with a distinct burst of firing for each pulse. At SPs of 200 ms or more, no decrement occurs (Fig. 8).

Regulation of the phonotactic threshold of the female cricket, Acheta domesticus : juvenile hormone III, allatectomy, L1 auditory neuron thresholds and environmental factors

Abstract Juvenile hormone III (JHIII), when applied to the abdomen of 1-day-old female Acheta domesticus (in quantities that would create JHIII titers in the hemolymph that were within the range measured in females of this species) caused a significant decrease in phonotactic thresholds (Fig. 1). Removal of the corpora allata from 5-day-old females with low phonotactic thresholds caused significantly increased phonotactic thresholds 2–5 days later. After a temporary increase (24 h) of, on average, about 25 dB, the phonotactic thresholds drop to about 10 dB above preallatectomy levels (Fig. 2), but remain significantly higher than controls. Application of JHIII to allatectomized females, with a mean increase in thresholds of 20 dB, results in significantly decreased thresholds (mean of about 20 dB) over the next 6 h (Fig. 3). Exposure to males 1 week before the imaginal molt causes the phonotactic thresholds of postimaginal females to drop 1–2 days significantly earlier than controls (Fig. 4). One- and 3-day-old females, phonotactically tested only once, exhibit lower thresholds in the early morning than they do in the late afternoon (Fig. 5). Five-day-old females do not exhibit such a diurnal rhythm. Phonotactically testing females more than once a day significantly influences their phonotactic thresholds (Figs. 6, 7). In 1-day-old females, with high (above 70 dB) phonotactic thresholds, the threshold of their L1 auditory interneurons can be 30 dB or more below their phonotactic threshold (Fig. 8). In females with phonotactic thresholds of 70 dB or lower, the L1 threshold is within 10 dB of their phonotactic threshold. Both JHIII and allatectomy influence phonotactic and L1 thresholds in a similar manner.

The effect of visual input on calling song attractiveness for female Acheta domesticus

ABSTRACT. Of twelve mature phonotactically‐responsive female Acheta domesticus L., ten responded phonotactically to a wider range (30 or SO to 100 ms) of model calling song (CS) syllable periods (SP) on the Kramer treadmill in the dark than in a lighted visually structured arena (50–70 ms). When given a choice between the visually attractive target and the invisible loudspeaker, seven of the ten females that tracked a visually attractive target (black square) when presented alone in the light reduced the range of SPs they tracked phonotactically to 50–70 ms. Three of the ten females that were not strongly attracted to the visual target when presented alone, continued to respond to model calling songs with a wide range of SPs (30–100 ms) when given a choice between visual and acoustical targets under the same conditions. Two of the twelve females responded only to model calling songs with a 50–70 ms SP on the Kramer treadmill in the dark. These females did not change their choice for model calling song SPs when presented with the visually attractive target.

Female Acheta domesticus track acoustical and visual targets with different walking modes

ABSTRACT. Female Acheta domesticus L. were tested for tracking model calling songs with different syllable periods on the Kramer treadmill in the dark, under homogenous light, and in the presence of a visually attractive target (black square) positioned either perpendicular to or in front of the invisible acoustical target. The females exhibited tracking of the two targets by different walking modes.

Morphology and physiology of local auditory interneurons in the prothoracic ganglion of the cricket Acheta domesticus

The omega-neuron 2 (ON2) is an auditory interneuron in Acheta domesticus that could play an important role in prothoracic auditory information processing. ON2 neurons were intracellularly recorded and iontophoretically stained with lucifer-yellow. The morphology of ON2 is similar to that described in other cricket species. Wholemounts and transverse sections of prothoracic ganglia show that ON2 branches cover the same regions as the omega-neuron 1 (ON1) branches except that ON2 has crossover branches in the anterior ring tract from both the ipsilateral and contralateral side. Auditory responses of ON2 are measured with spiking thresholds of about 60 dB SPL at 16 kHz (courtship song frequency) and about 80 dB SPL at 5 kHz (calling song frequency) under open field and closed field (monaural) stimulation. Open and closed field stimulations show almost identical threshold curves and response magnitudes to soma-ipsilateral and soma-contralateral stimulation. These data do not support a function of ON2 for directional hearing. In addition to excitation, ON2 receives inhibitory inputs from both ears at 5 and 16 kHz. Subthreshold inhibition is obvious in responses with open and closed field stimulation at 5 kHz. Responses show mixed excitation and inhibition at intensities above 80 dB SPL at 5 and 16 kHz. These data confirm previous immunohistochemical results showing GABAergic input to ON2 in Gryllus bimaculatus. Two newly described local neurons (“LN1”, “LN2”), which are probably nonspiking and have low 5-kHz thresholds, could be candidates for the inhibitory input to ON2. J. Exp. Zool. 279:43-53, 1997.© 1997 Wiley-Liss, Inc.

Low-pass filtering of sound signals by a high-frequency brain neuron and its input in the cricketAcheta domestica L.

Summary1.The morphology and response properties of a high-frequency, bilaterally projecting brain neuron (HBB1) is described for the cricketAcheta domestica.2.HBB1 has processes in several regions of the protocerebrum (Fig. 1), many of which overlap those of L3, an ascending prothoracic interneuron (Fig. 7).3.HBB1 is most responsive to 16-kHz sounds (Fig. 2), but only responds to suprathreshold signals with 1–3 spikes/syllable (Fig. 5). HBB1 also receives inhibitory input following excitation (Fig. 4). If the syllable period (SP) of the chirp is less than 95 ms, HBB1 only produces action potentials in response to the first syllable of the chirp, whereas a chirp having SPs greater than 160 ms induces spiking to each syllable, i.e., a low-pass filter (Figs. 3, 6).4.Several correlations exist between the input excitatory postsynaptic potentials of HBB1 and the spiking of L3. These findings are consistent with L3 providing auditory input to HBB1 (Figs. 8–10).5.The suggestion of HBB1 being involved in courtship song filtering is discussed.