Studies of the Neural Basis of Evasive Flight Behavior in Response to Acoustic Stimulation in Heliothis zea (Lepidoptera: Noctuidae): Organization of the Tympanic Nerves

Abstract

The organization of the tympanic nerve within the thoracic ganglia of Heliothis zea (Boddie) was investigated. Cobalt chloride infiltration of cut axons was used to investigate the central terminations of the tympanic nerves. The axonal terminals of the A2 acoustic cell were confined to the meso-metathoracic ganglia, whereas the Al acoustic and the nonacoustic B cell were found in the thoracic ganglia. The relevance of this organization for neural circuitry of evasive flight behavior to acoustic stimulation is discussed.KEY WORDS Insecta, auditory processing, noctuid moths, neural circuits THE AUDITORY SYSTEM of. noctuid moths is especially amenable to experimental investigations because of its inherent simplicity and accessibility. Therefore, it serves well as a model system for understanding sensory processing in general, and particularly for studying the neural basis of evasive flight behaviors in insects. Each ear has only a single pair of acoustic cells, the Al and A2 cells, as well as a nonacoustic B cell. The acoustic cells are especially sensitive to ultrasound (10-100 kHz) and have response spectra nearly identical, except that the Al cell is about 20 dB more sensitive to sound pressure level at threshold (Agee 1967, Roeder 1975, Surlykke & Miller 1982. Our recent research at this laboratory has focused on the neural circuitry within the central nervous system (CNS) of the noctuid moth Heliothis zea (Boddie), known commonly as the corn ear worm or bollworm moth (Agee 1985, Orona & Agee 1988.The objective of this research on the auditory system was to understand better the axonal terminations and neural circuits of the acoustic nerves, so that areas within the ganglia of potential synaptic interaction with motoneurons could be identified. Understanding the neural coding within a simple sensory system should reveal general principles applicable to more complex systems. Our objective is to discover and understand the circuitry from the sensory inputs to the motoneurons that generate evasive flight behaviors, as has been attempted for the organization of auditory and motor circuits in locusts (Kien & Altman 1984, Boyan Mention of a commercial or proprietary product does not constitute an endorsement by the USDA. Materials and MethodsAdult male and female H. zea (3-4 d old) were reared in this laboratory. Tympanic nerves were infiltrated with a variation of the procedure of Tyrer & Altman (1974). The thoracic ganglia were exposed by dissecting from the venter. They were immersed in vivo in a drop of Carlson's saline until the ganglia and nerves were dissected free. Careful dissection allowed access to the penultimate branch of nerve IIINIB (nomenclature of Eaton 1974), which includes the acoustic nerves and those bearing motoneurons to some of the dorsal longitudinal muscles. Nerve trunks to be filled were left at their maximal lengths, and all others were cut proximal to the ganglia.Cobalt infiltration was performed in vitro on nerve IIINIB. Occasionally, we could infiltrate either of the two ...

Neurometamorphosis of the ear in the gypsy moth,Lymantria dispar, and its homologue in the earless forest tent caterpillar moth,Malacosoma disstria

“…If these organs are ontogenetically homologous, it follows that the neurons contained within them should reside in ontogenetically homologous regions of the CNS. As with the peripheral anatomy of the noctuoid moth ear, the CNS projection patterns o f its neurons were previously described (Paul, 1973;Surlykke andMiller, 1982: Agee andOrona, 1988;Boyan andFullard, 1988: Boyan et al, 1990), and the tympana1 cells of L. dispar adults do not noticeably differ from those reported for other noctuoids. As with noctuids (Surlykke and Miller, 1982), L. dispur's two auditory CO neurons (A1 and A2) and one nonauditory multipolar neuron ( B ) remain mostly ipsilateral within the pterothoracic ganglion after entering via the IIINl nerve.…”

Hearing and evasive behaviour in the greater wax moth, Galleria mellonella (Pyralidae)

“…It has been suggested that last chance evasive manoeuvres of noctuids are elicited by A 2 ‐cell activity directly through the meso‐ and metathoracic ganglion (Fullard, 1982; Boyan & Fullard, 1986; Agee & Orona, 1988). The situation appears to be different in greater wax moths.…”

Evolutionary escalation: the bat–moth arms race

“…The axons of these cells enter the pterothoracic ganglion located in the thorax (Surlykke and Miller, 1982), where they synapse with auditory interneurons (Boyan and Fullard, 1986). The A1 and B-cells have projections that either terminate in the pterothoracic ganglion or extend up to the suboesophogeal ganglion, whereas A2 projections are limited to the pterothoracic ganglion (Agee and Orona, 1988;Zhemchuzhnikov et al, 2014). The exact circuitry involved in processing auditory inputs is unknown in moths, although models have been proposed (Boyan and Fullard, 1986;Boyan et al, 1990).…”