Simple ears – flexible behavior: Information processing in the moth auditory pathway

Abstract

Lepidoptera evolved tympanic ears in response to echolocating bats. Comparative studies have shown that moth ears evolved many times independently from chordotonal organs. With only 1 to 4 receptor cells, they are one of the simplest hearing organs. The small number of receptors does not imply simplicity, neither in behavior nor in the neural circuit. Behaviorally, the response to ultrasound is far from being a simple reflex. Moths' escape behavior is modulated by a variety of cues, especially pheromones, which can alter the auditory response. Neurally the receptor cell(s) diverges onto many interneurons, enabling parallel processing and feature extraction. Ascending interneurons and sound-sensitive brain neurons innervate a neuropil in the ventrolateral protocerebrum. Further, recent electrophysiological data provides the first glimpses into how the acoustic response is modulated as well as how ultrasound influences the other senses. So far, the auditory pathway has been studied in noctuids.The findings agree well with common computational principles found in other insects. However, moth ears also show unique mechanical and neural adaptation. Here, we first describe the variety of moths' auditory behavior, especially the co-option of ultrasonic signals for intraspecific communication. Second, we describe the current knowledge of the neural pathway gained from noctuid moths. Finally, we argue that Galleriinae which show negative and positive phonotaxis, are an interesting model species for future electrophysiological studies of the auditory pathway and multimodal sensory integration, and so are ideally suited for the study of the evolution of behavioral mechanisms given a few receptors [Current Zoology 61 (2): 292-302, 2015].

Search calls long duration puts the bat on the tympanate moth's radar. A new perspective on how Noctuoidea's auditory cells drive evasive manoeuvres

“…Fullard's interpretation that the A cell encodes the pulse repetition rate did explain that some moth species exploit the pulse repetition rate to distinguish between bat calls and mating calls [23]. Our interpretation suggests that the exploitation of the pulse rate may take place at the interneuron level [5,24].…”

“…It also opens a host of possibilities for the potential parameters involved in the moth's calculations besides pulse intensity: pulse duration, pulse repetition rate, pulse carrier frequency, and integration over time. The actual combination remains to be determined in order to understand how the complex survival behaviours of the moth are elicited with -for some of them -only one neuron bridging the environment and the nervous system [5].…”

Ear-Bot: Locust Ear-on-a-Chip Bio-Hybrid Platform

“…Hearing evolved multiple times in insects [ 11 ] serving the functions of scene analysis and communication. Insect auditory sensors are highly diverse (1) in morphology—insect ears range from near-field sensitive antennae to far-field sensitive tympanic membranes 11 ; (2) in function—ranging from narrow band filters (e.g., in mosquitos [ 12 ]) to wide-band sensors (e.g., in noctuid moths [ 13 ]) and (3) in neural processing—ranging from one neuron ears (e.g., in noctuid moths) to ears with thousands of intervening neurons (e.g., 15,000 in the male mosquitos). Several recent studies applied bio-inspired phonotaxis in robots, equipped with acoustic electronic sensors used to identify and respond to sound [ 14 , 15 , 16 , 17 , 18 , 19 ].…”

Prolonged Bat Call Exposure Induces a Broad Transcriptional Response in the Male Fall Armyworm (Spodoptera frugiperda; Lepidoptera: Noctuidae) Brain

“…Often before a predator has even localized its prey, a suite of adaptive behavioral and physiological responses which improve the chances of survival (Endler, 1991) are induced in prey organisms which may be eavesdropping on mechanical, auditory, visual, and chemosensory predation cues (Adamo et al, 2013). For instance, moths and butterflies that are sensitive to ultrasound display startle responses when exposed to synthetic broad frequency ultrasound (Roeder, 1966; Ratcliffe et al, 2008, 2011; ter Hofstede et al, 2011) and recorded bat calls (Acharya and McNeil, 1998; Rydell et al, 2003; Ratcliffe and Fullard, 2005), such as changing the course of flight, ceasing flight, accelerating, performing evasive flight maneuvers (Yack, 2004; Yack et al, 2007; Pfuhl et al, 2015), and/or calling back with jamming ultrasound themselves (Corcoran et al, 2009). Upon exposure to ultrasound, non-flying noctuid moths cease movement while many aerial noctuids exhibit evasive flight maneuvers, such as erratic changes in direction, loops, increases in flight velocity, and even falling to the ground (Surlykke and Miller, 1982).…”