Neuroendocrine Regulation of Animal Vocalization: Mechanisms and Anthropogenic Factors in Animal Communication

Neuroendocrine Regulation of Animal Vocalization: Mechanisms and Anthropogenic Factors in Animal Communication examines the underpinning neuroendocrine (NE) mechanisms that drive animal communication across taxa. Written by international subject experts, the book focuses on the importance of animal communication in survival and reproduction at an individual and species level, and the impact that increased production and accumulation of endocrine-disrupting chemicals (EDCs) can have on these regulatory processes.

This book discusses sound production, perception, processing, and response across a range of animals. This includes insects, fish, bats, birds, nonhuman primates, infant humans, and many others. Some chapters analyze how neuroactive substances, endocrine control, and chemical pollution affect the physiology of the animal’s perceptive and sound-producing organs, as well as their auditory and vocal receptors and pathways. Other chapters address the recent approaches governments have taken to protect against the endocrine disruption of animal (vocal) behaviors. The book is a valuable resource for researchers and advanced students seeking first-rate material on neuroendocrinological effects on animal behavior and communication.

• Serves as the most comprehensive cross-taxa study of its kind, revolutionary in its focus on the impacts of EDCs on the processes guiding animal communication
• Emphasizes the importance of production, perception and processing of acoustic vocalization for survival
• Analyzes recent governmental policies and protections against the effects of EDCs on humans and wildlife

• Language: English
• Publisher: Academic Press
• Release date: Dec 4, 2020
• ISBN: 9780128151617

Book preview

Part I

Introduction

Chapter 1: Neuroendocrine control of sound production and perception

Sakina Mhaouty-Kodja    CNRS, INSERM, Neuroscience Paris-Seine—Institute of Biology Paris-Seine, Sorbonne University, Paris, France

Abstract

Communication between individuals through sound production by a sender and integration by a receiver is highly used in the animal kingdom from invertebrates to vertebrates. It is used in different contexts, in particular during the reproductive period where it plays a crucial role in bringing together sexual partners. The endocrine regulation by sex steroid hormones of both sound production and perception has been reported in fish, frogs, birds, and rodents, although the neural signaling pathways still need to be documented in several species. In this context, whether and how such communication can be altered by exposure to environmental chemicals able to interfere with hormonal systems is a relevant question that is being recently asked in the field of endocrine disruption.

Keywords

Sound production; Sound perception; Vocalizations; Neuroendocrine regulation; Sex steroid hormones; Endocrine disruptors

Communication between animals involves the transmission of signals from senders to target receivers. These signals can be chemical, visual, tactile, or acoustic. Sound is produced by a variety of invertebrate and vertebrate species. Nonvocal sound among insects include those produced through external body structures such as tymbals attached to both sides of a cicada’s abdomen or the stridulatory organ of crickets. Some vertebrate species also produce nonvocal sounds with their feet, wings, tails, or by bill clattering as in the oriental white stork, Ciconia boyciana. Furthermore, in many vertebrates vocal sounds are produced under muscular control, by a vibrating membrane located in the syrinx in birds or the larynx in frogs, toads, some reptiles, and mammals. These sounds present different species-dependent features and even individually distinctive patterns in the same species have been reported across all classes of vertebrates. The sound produced by a sender is integrated by the receiver and is translated into adaptive behavior. It is mainly used in social contexts of intraspecific communication. Interactions between individuals can occur starting at an early age, such as the ultrasonic calling by isolated rodent pups that elicits pup retrieval activity by mothers. Sound can also be used during interactions between either juveniles or adult individuals of the same or opposite sexes. Sound used in the context of male-female interaction during courtship is among the most studied behavior in invertebrate and vertebrate species. The research on this aspect has largely addressed the factors modulating the production and perception of sound by sexual partners.

Seasonal and endocrine regulation of sound production and perception

Sound production is finely regulated by both external and internal factors. Among the external factors, seasonal variation is often associated with changes in sound production. Indeed, several animal species that exhibit seasonality in reproduction modulate their acoustic signals seasonally, with increased sound production rates during the breeding season. Animal models for seasonal variation in sound production related to courtship exist across multiple species ranging from fish and amphibians, through birds, where extensive studies have been performed, to mammals. The internal factors relate essentially to the gonadal hormone status, which in seasonally breeding species is also dependent on seasonal variation. Even in laboratory rodents that have almost lost the seasonal regulation of reproduction, the majority of studies show that the emission of ultrasonic vocalizations during the precopulatory phase is closely dependent on gonadal hormones (for review, Ref. [1]). The endocrine regulation of sound production has been widely demonstrated in the context of reproductive behavior in fish, frogs, birds, and rodents. Sex steroid hormones appear as the main modulators of the information content of vocal signals. In male fish and amphibians, gonadal testosterone acts on peripheral musculature and on neural structures either directly or indirectly following metabolization into neural estradiol to influence the vocalization rate, duration, and amplitude [2–4]. Vocal behavior presents a high level of plasticity in response to the stimuli emitted by females. For example, the ultrasonic vocalizations of male rats or mice are stimulated by female olfactory cues, with the highest rates of ultrasonic vocalizations produced in response to estrous females [5].

Endocrine coupling of seasonal reproduction to adaptive behavioral plasticity has also been shown for sound perception. In the plainfin midshipman fish, Porichthys notatus, the seasonal onset of male calling coincides with an increased sensitivity of the female auditory system to detect and respond to singing males [6–8]. Perception of auditory information was also found to be enhanced in sexually receptive females of cichlid fish [9]. In both species, specific neuroendocrine mechanisms involving gonadal sex steroids underlie these changes in perception. Evidence for a potent role of sex steroids in regulating signal perception of male calls by females was also reported for frogs [10], birds [11–13], and rodents [14].

Gonadal hormones are therefore key regulators of acoustic communication across species, in particular in the context of reproduction. However, it is important to mention that other endocrine factors have been also suggested for the regulation of vocal communication, although they remain less studied than sex steroid hormones. In the brain of the green damselfish, Abudefduf abdominalis, different forms of hypothalamic gonadotropin-releasing hormone (GnRH) exist and act as neuromodulators. Electrophysiological studies have shown that this neuropeptide influences context-specific auditory processing, suggesting a potential role in the modulation of seasonal auditory-mediated social behavior [15]. Evidence has been also reported for the relevant roles of stress hormones in particular in fish [9, 16–18].

Neuroendocrine regulation of sound production and perception

The roles of sex steroids in reproduction are conserved across species. Their synthesis and secretion by gonads are under the control of GnRH, which stimulates synthesis and secretion of pituitary luteinizing hormone and follicle stimulating hormone that will in turn increase the gonadal production of sex steroids. This hypothalamic-pituitary-gonad axis is crucial for the expression of male and female reproductive behavior. Testosterone and estradiol start shaping the neural structures underlying behavioral responses during the early developmental stages. This results in a permanent organization of the neural circuitry underlying sexual behavior at the neuroanatomical and molecular levels. In rodents, sex differences in cell number and morphology, in fiber density or in gene expression have been observed along this circuitry from the chemosensory medial amygdala and bed nucleus of stria terminalis to the hypothalamic preoptic or ventromedial areas [19], where signals are processed into behavioral responses. In male birds and rodents, the motivation to sing seems dependent on the medial preoptic nucleus [20–22]. It remains to be documented whether and how this structure is connected to the motor system involved in sound production and performance including forebrain and midbrain sensorimotor integration centers, hindbrain and spinal cord motor centers, and muscles.

Sex steroids are also required during adulthood to activate the expression of male- and female-typical behavior. The organizational and activational effects of testosterone and estradiol involve mainly the androgen and estrogen receptors, respectively. In the male nervous system, gonadal testosterone activates the androgen receptor, but it can also be metabolized into neural estradiol, which stimulates the estrogen receptors. These receptors belong to the superfamily of nuclear hormone receptors and exert genomic effects through transcriptional regulation of target genes.

The early organization and adult activation by sex steroids seems to apply to vocal communication in frogs, birds, and rodents. In Xenopus laevis, testosterone and its metabolite estradiol act during periods of both organization and activation on several sites including the sensorimotor and motor centers, to regulate courtship vocalizations [23]. In songbirds, the recent review by Alward et al. [24] provides a good summary of the multiple neural sites of action for both androgens and estrogens. Androgen receptors are expressed early during canary brain development and their expression persists throughout life in song-control nuclei and in the medial preoptic area, suggesting that steroid hormones acting through androgens are important for early vocal learning and later vocalizations. In this model, the expression of estrogen receptors is restricted to the HVC nucleus. In gerbils, injection of testosterone to female neonates masculinizes and defeminizes ultrasound emission rates in juvenile animals [25].

The activational effects exerted by sex steroids during adulthood to modulate sound production have been also largely described in various species (for reviews in fish: Ref. [6]; frogs: Ref. [23]; songbirds: Ref. [24]; and rodents: Ref. [1]). For example, testosterone implants in specific brain regions of castrated male canaries showed that the medial preoptic area is a key structure where testosterone acts to increase song rate and activate copulation, but its action in other areas of the brain or periphery is also necessary to enhance the quality of song and regulate context-specific vocalizations [26]. In rodent models, ultrasonic vocalizations emitted by males during mating are completely restored in castrated mice receiving implants of testosterone into the medial preoptic area but not in the corticomedullar amygdala, septum, anterior and ventromedial hypothalamus, or ventral tegmental area [27–30]. Estradiol benzoate implanted into the preoptic area also activates the emission of ultrasonic vocalizations in male mice and gerbils [28, 31]. In male mice, the involvement of neural androgen receptors in testosterone-induced regulation of ultrasonic vocalizations was recently demonstrated using a transgenic model lacking the gene encoding this receptor in the nervous system. Mutant males displayed a smaller total number and shorter duration of ultrasonic vocalizations in the presence of receptive females than their control littermates [32].

Hormonal modulation of neural structures that process auditory information has been demonstrated in several vertebrate species. The first evidence of androgen-containing neurons in a midbrain nucleus stimulated by sound was reported in X. laevis [33]. Further studies in songbirds revealed the presence of aromatase and estrogen receptors in both the peripheral auditory system [34] and auditory forebrain [35–38], with response properties of the auditory forebrain modulated by the season [39] and estrogens [12, 40–42]. Similarly, the presence of sex steroid receptors was reported in the fish auditory system, with mRNA levels varying according to the hormonal state and social status (reviewed in Ref. [43]).

Besides the long-term effects induced by sex steroids through the regulation of genomic pathways, data support the idea that these hormones can also induce rapid changes in sound production and perception possibly through the activation of membrane-bound receptors. Studies in songbirds have shown that testosterone and its estrogen metabolites are able to rapidly regulate birdsong motivation and performance in males (reviewed in Ref. [24]), and that estradiol enhances the responsiveness and coding efficiency of auditory neurons in females (reviewed in Ref. [13]). Furthermore, testosterone and estradiol were also able to rapidly modulate the duration and frequency of ultrasonic vocalizations in male hamsters, suggesting an action through cell membrane receptors [44].

Does environmental exposure to endocrine-disrupting compounds affect sound production and perception?

The previous paragraphs summarize the tight regulation of sound production and perception by gonadal hormones, in particular during the reproductive period. This suggests that any potential alteration in the concentrations of these hormones or in their signaling pathways could interfere with the expression of such behavior.

The worldwide decline of wildlife observed over the past few years seems to be due to several factors including overexploitation, loss of habitat, climate change, and chemical contamination [45]. The past decades witnessed a massive increase of production of chemicals used in several human activities. Among those chemicals, molecules that interfere with hormonal systems are defined as endocrine-disrupting compounds (EDC). According to the definition of the World Health Organization [45]: An endocrine disruptor is an exogenous substance or mixture altering the functions of the endocrine system, and thus inducing adverse health effects on an intact organism, its offspring, or within subpopulations. This alteration may target hormonal synthesis, release or metabolism, hormonal binding to receptor or receptor expression levels. EDC present in the environment can be naturally occurring (phytoestrogens present in plants, human, and animal steroid hormones released into wastewater and rivers). However, man-made compounds represent a large panel of products including molecules used in agriculture [pesticides such as dichlorodiphenyltrichloroethane (DDT), fungicides like vinclozolin] or industry [plasticizers such as bisphenols or phthalates, polychlorinated biphenyl (PCB) or polybrominated diphenyl ethers are used as flame retardants]. Some of these compounds like DDT or PCB are persistent organic pollutants. They have been banned since the 1970s and 1980s but are still detected in the environment and in biological samples derived from wildlife and humans.

In the landmark book Silent Spring published in 1962 [46], Rachel Carson was the first biologist to draw attention to the dangers inherent in the ubiquitous release of DDT into the environment because this is an insecticide that interferes with reproductive and thyroid systems. She highlighted several points that are particularly relevant at the present time: low doses of chemicals can have significant effects on exposed animals, chemical mixtures can lead to aggravated effects, and effects may change depending on the period of life when exposure takes place. Since her work, a multitude of studies reported a link between exposure to EDC and alteration of reproductive functions in wildlife [45]. Experimental studies conducted on laboratory animals confirmed effects on development, reproduction, metabolism and behavior. Several reports showed effects at low doses—below the reference doses estimated from toxicological studies, with nonmonotonic dose responses in some cases.

In this context, the potential effects of exposure to EDC on animal acoustic communication remain poorly explored, although reproductive behavior has been widely assessed (for reviews in rodents: Refs. [1, 47]). Furthermore a special interest has been given to developmental and pubertal periods because exposure to EDC during these sensitive periods may induce long-lasting effects and promote epigenetic transgenerational modifications. However, it is now widely established that the adult brain retains plasticity and that several environmental factors can also affect neural structure and function. Indeed, adult exposure to environmental doses of a plasticizer phthalate alone, an alkylphenol-derived molecule (nonylphenol) alone, or combined exposure to both molecules were shown to trigger significant modifications in the emission of ultrasonic vocalizations by male mice during courtship [32, 48, 49].

Given the importance of acoustic communication in social behavior including mating approaches, more attention should be focused on the assessment of the effects of exposure to endocrine disruptors on sound production and perception. Of necessity, this involves a better understanding of the mechanisms underlying the hormonal regulation of such behavior. Bringing together the latest knowledge on this neuroendocrine regulation from invertebrates to vertebrates and the pilot works on the effects and mechanisms of EDC exposure, as it is proposed here, represents an excellent initiative. It will probably shed light on this behavior that is not yet much studied in the field of endocrine disruption.

References

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Part II

Sound Production and Perception

Section A

Invertebrates

Chapter 2: Regulation of acoustic sensory-to-motor processing in insects

Ralf Heinricha; Andrea Wirmerb    a Department of Cellular Neurobiology, University of Göttingen, Göttingen, Germany

b Institute of Neurobiology, Ulm University, Ulm, Germany

Abstract

Acoustic communication in insects serves mate attraction, courtship, aggregation, competition, territoriality, and predation and may inform a conspecific receiver about the physiological status of the sender. Acoustic signals are associated with particular behaviors and should only be performed in the correct context. This context is internally represented by neuroendocrinal signals. Hormones released from endocrine organs and neurosecretory regions establish or reconfigure neural circuits and determine general physiological states, which represent permissive requirements for the execution of a particular behavior that may include sound production. Neuromodulators alter the sensitivity of sensory and decision making premotor circuits to regulate the likelihood, specific pattern and intensity of sound production or other behaviors on a minute timescale. Neurotransmitters serve as immediate triggers for the initiation of sound production in response to actual sensory input and mediate the fine-tuned synaptic transmission in pattern-generating circuits. Different aspects of the neuroendocrinal regulation of acoustic sensory-to-motor processing have been studied in relatively few insect species, most intensively in grasshoppers, crickets, bushcrickets, honey bees, and fruit flies.

Keywords

Insect; Acoustic communication; Hormone; Neuromodulator; Neurotransmitter; Actual environment; Physiological state; Social behavior

Introduction

Insects represent the most speciose group of animals. Oldest fossils of insects date back more than 400 million years [1] and fossil proof for sound-producing stridulation organs indicate that acoustic communication among insects was already established 165 million years ago [2]. Intraspecies communication and predator detection served as major driving forces for the evolution of hearing organs [3, 4]. While most insects are deaf, 9 out of ~  30 orders contain species with sound-sensitive ears [5]. Various types of hearing organs emerged multiple times at different locations on the insect body [6–8]. Neural circuits for sound production probably evolved from neuronal substrates that previously regulated ventilation, because pattern generating circuits underlying rhythmic sound generating movements are distributed over posterior thoracic and anterior abdominal ganglia, even when sound producing body parts are located in different segments [9].

Acoustic communication in modern insects serves mate attraction, courtship, aggregation, competition, territoriality, and predation [10]. Acoustic behaviors, including both sound production and sound perception-triggered actions, are regulated by neuroendocrine processes which initiate particular behavioral acts only in appropriate situations [11, 12]. These appropriate situations are determined by both the actual sensory environment represented by the entirety of sensory input and the internal physiological state of the individual. Investigation of neuroendocrinal signaling, serving as an internal representation of physiological state and external situation, is always confronted with the problem that any manipulation (e.g., handling, restraining in experimental setup, and taking samples) changes the situation and hence distorts the composition of regulatory chemical messengers.

Acoustic communication in insects

Insects communicate through visual, olfactory, vibrational, and acoustic signals [13]. Extant species use various modes for sound production and harbor various types of auditory receptors at different locations on their bodies. Insects are challenged with diverse tasks that include identifying and locating conspecifics, finding food resources and avoiding predation. Acoustic signals may (1) address other species to startle, warn, or disturb predators [14–17]) or (2) may be used for intraspecies communication, to aggregate conspecifics [18], attract mating partners, or establish mating readiness [19, 20]. Species- and context specificity of insect acoustic communication signals is typically contained in their temporal patterns [21]. These patterns may contain information about gender, size, physiological state, and other qualities of the sender [22–25].

Sound production

Acoustic signals of insects cover a frequency range from below 100 Hz to 150 kHz, reach intensities of up to 120 dB SPL and enable communication distances from less than 1 cm (fruit flies) up to several hundred meters (bladder grasshoppers, mole crickets, and cicadas). Airborne sounds and substrate vibrations are generated by different mechanisms, propagate through the air or solid substrate with different characteristics and are detected by auditory receptors tuned to respective physical characteristics. In the far field (distance larger than two times the wavelength) air-borne sound travels as nearly plane pressure waves with predictable reduction of intensity with increasing distance. Near field sound, close to the source, lacks a fixed relationship between pressure and distance, attenuates rather quickly and is dominated by motion of air particles. Substrate vibrations strongly depend on the solidity and resonant characteristics of the substrate.

Dipterans produce sounds by wing vibration [25–27]. Signals of aggression and courtship by males have been studied especially in Drosophila [28–30]. Bees produce air-borne signals by rhythmic oscillations of their thorax [13, 31]. Other insects possess dedicated stridulatory organs consisting of a cuticular ridge (scraper) on one part of the body that is scraped over a toothed ridge (file) on another part. Stridulatory apparatuses can be found at various locations on the body. In ants, two tergites of the gaster are scraped against each other [32, 33], some beetles possess a stridulatory apparatus between pronotum and thorax [34], whereas in crickets and bushcrickets, scraper and file are veins of the forewings and sounds are produced by rubbing the wings against each other [35–39] (Fig. 1A–C). Acridid grasshoppers [40, 41] and some moths [42] scrape their legs against their wings to produce sounds (Fig. 1D and E). Other behaviors include the following: percussion, drumming parts of the body against each other or against the substrate, as in ants and wingless termites [43, 44], air expulsion, expelling air at high pressure through the tracheal spiracles, found in the Madagascar hissing cockroach [45] and click mechanisms, buckling of a membrane between two stable positions, as applied by cicadas [46]. Vibrations of solid substrate represent an additional or exclusive channel of information that various insects use in intraspecific communication. Most behaviors leading to sound production result in both, air-borne and substrate-borne signals [47]. The muscles that drive the sound producing movements are typically activated by pattern generating networks located in one or more ganglia of the central nervous system [48–50]. It has been demonstrated in various insects (including crickets, grasshoppers, and fruit flies) that these pattern generating networks are activated by descending brain neurons which in turn are activated by brain-internal decision-making circuits [50–54].

Fig. 1

Fig. 1 Sound production in orthopterans. (A) A stridulating male cricket rubs its fore wings against each other. (B) Fore wing of male cricket ( Gryllus campestris ). Areas like harp and mirror cells provide characteristic resonance features to the wing. (C) Cricket sound production mechanism. The plectrum of the left wing is scratched against the teeth of the file on the underside of the right wing. (D) Grasshoppers produce sounds by rubbing their hind legs against the fore wings. (E) Stridulatory apparatus of acridid grasshoppers. Stridulatory pegs on the carinula at the inner side of the femur are rubbed against the protruding intercalary vein of the fore wing. Scale bars: 10 mm.

Sound perception

Insect hearing organs fall into two principal categories [5, 55]: tympanic organs that typically include regions of thin cuticle (tympanic membranes) backed by air-filled structures which vibrate in response to sound pressure fluctuations [6, 56] (Fig. 2A and B) and antennal ears (e.g., Johnston’s organ in dipterans) that respond to particle movement in the acoustic nearfield [57, 58] (Fig. 2C). In addition, filiform hairs located on cerci, antennae, or other parts of the body may also be deflected by sound particle displacement [59, 60]. Hearing organs typically are chordotonal organs composed of one to several thousand scolopidia, each consisting of one or more sensory neurons, scolopale (envelope) cells, and a cap cell (Fig. 2D). Insect ears are sensitive to frequencies of less than 100 Hz up to 300 kHz [6,56,61–63]. Sound particle movement detectors typically respond to frequencies below 1–2 kHz while pressure and pressure gradient receivers detect sounds of higher frequencies. Sensitivity in the far ultrasonic range is typically related to bat avoidance, enabling evasive responses on detection of hunting bats’ echolocation calls [64]. Tuning of auditory receptors to particular frequencies has been described in many species [65–68] and typically arises (as in vertebrates) from properties of accessory structures (e.g., regional stiffness of tympanal membranes, dampening of sound entry, and sound propagation to auditory neurons) rather than from intrinsic properties of auditory receptors.

Fig. 2

Fig. 2 Sound perception in grasshoppers and dipterans. Hearing organs typically are chordotonal organs composed of one to several thousand scolopidia, each consisting of one or more sensory neurons, scolopale cells and a cap cell. (A) Schematic view of the auditory ganglion (Müller’s organ) attached to the tympanum by sclerotized processes: the elevated process, styliform body, pyriform vesicle, and folded body. Vibrations of the tympanum excite mechanosensitive receptor neurons within these processes. Their axons build the auditory nerve. (B) A group of scolopidia within the auditory ganglion elevated process. Cap cells connect auditory receptors to the tympanic membrane. (C) Johnston’s organ at the antennal base of a fruit fly. Rotations of the third antennal segment (a3) excite scolopidial sensory neurons located in the second antennal segment (a2). Sound deflects the arista leading to a rotation of a3 and a mechanical deflection of scolopidia. (D) Left : Monodynal scolopidium as found in the Müller’s organ of locusts. Right : Heterodynal scolopidium as found in the Johnston’s organ of dipterans.

Sensory-to-motor processing of auditory information

Auditory receptor cells have evolved from mechanoreceptors [56] and are primary sensory cells that project axons (typically cholinergic) into mechanosensitive central nervous neuropils dedicated for the processing of auditory information [69]. Auditory receptor axons enter the ganglion (or the neuromere in case of fused ganglia) of the same body segment where the ear is located and terminate in primary auditory neuropils in the same or adjacent ganglia [5,70–72]. Accordingly, primary auditory neuropils of acridid grasshoppers (hearing organs in first abdominal segment) are located in the third thoracic ganglion complex [73, 74], those of crickets and bushcrickets (hearing organs in the front legs) in the first thoracic ganglion [75] and those of fruit flies and honeybees who hear with Johnston’s organs in the antennae are located in the deutocerebrum of the brain [58, 76, 77]. Local interneurons may process auditory information to enhance directionality of bilaterally perceived acoustic signals [8], to restrict frequency bands by inhibition or to extract particular features of detected sounds [71, 78, 79]. Other interneurons typically relay this preprocessed auditory information to brain-located neural filters for pattern recognition and feature analysis [74, 80]. First steps of frequency analysis take place on the level of the primary auditory neuropil enabling ascending interneurons to be tuned to frequencies of conspecific sounds [78]. In various orthopteran species, the important neurons for pattern recognition have been localized within lateral protocerebral regions of the brain [81–85] and in some noctuid moth species, ascending interneurons were found to arborize in the ventrolateral protocerebrum [86]. The mechanisms of pattern recognition are poorly understood and are best studied in orthopteran species like crickets and grasshoppers [78, 84, 87, 88] and Drosophila [89–91].

In crickets, sound features like direction and frequency are preprocessed in the primary auditory neuropil. A well-studied neuron is the omega neuron (see Fig. 5) that accurately transmits the temporal patterns of sounds in the frequency range of cricket calling songs and bat echolocation calls [92]. Ascending auditory interneurons with somata located in the prothoracic ganglion arborize in the lateral accessory lobes of the protocerebrum [88]. Local neurons in this region form small networks that recognize the pulse pattern of field cricket calling songs on the basis of characteristic synaptic delays and coincident activation of interneurons [87]. A different mechanism that relies on resonant membrane properties of higher order auditory interneurons has been shown to serve calling song recognition in a bush cricket [93].

Little information exists about the sensory-to-motor coupling which mediates appropriate responses to perceived acoustic signals, like response songs in duetting species [94], phonotaxis toward calling mates [88, 95] or avoidance of echolocating bats [96]. Integration of sensory inputs with signals representing an individual’s physiological state finally selects the appropriate behavior from the species-specific repertoire of motor patterns and physiological regulations.

Neuronal control of acoustic communication

Insects typically contain segmented central nervous systems, with one ganglion per body segment. However, supraesophageal ganglia (brain), subesophageal ganglia and terminal ganglia consist of multiple neuromeres that arose from fusion of individual ganglia. Concerning thoracic and abdominal ganglia, the degree of fusion can be quite different among species, resulting in only one thoracoabdominal ganglion in extreme cases (e.g., in dipteran flies) [97, 98]. Ganglia (or neuromeres) house pattern generating interneurons and motorneurons that control muscles of the same segment and they also receive (and often process) sensory input from sensory cells located in their segment [99–102]. As an example, the prothoracic ganglion of crickets (Fig. 5) and bushcrickets contains neural circuits which generate neuro-muscular excitation patterns of the front legs for walking and grooming [103, 104]. It receives sensory input from auditory organs in the front legs and processes this information in a dedicated auditory neuropil located in the anterior part of the ganglion [8,78,105–108]. Sensory information is typically relayed through multisegmental ascending interneurons to brain ganglia [96, 108], where further processing and analysis may occur, before information of different modalities and from different parts of the body converges in higher associative brain neuropils such as the mushroom bodies or the central complex [109]. These associative brain neuropils are considered as decision-makers [110] that activate (either directly or indirectly) descending pathways which in turn stimulate the premotor circuits in segmental ganglia and lead to the execution of particular motor programs [82, 111, 112]. In addition to sensory information (visual, mechanosensory/auditory, olfactory, etc.) that reflects the actual environment of the insect, selection of behavior also depends on memory related to previous experiences and the physiological state determined by factors including development and maturation, metabolic situation, reproductive cycles, and other biological rhythms. Physiological states typically change with slower rates (compared with sensory input from actual environment) and are represented by hormonal signals or longer-lasting neuromodulatory systems [11,113–116]. Hormones influence behavior in insects. Octopamine and other biogenic amines are involved in the modulation of complex behaviors like aggression [117] and influence stereotypic movements like flying [118] or grooming [119]. Juvenile hormone (JH) is a regulator of reproduction-related behaviors [120–123] but can also increase motor neuron activity [124] or change the insect’s sensitivity to sensory stimuli [125]. It has been demonstrated in numerous experiments that neurons in the central nervous system express specific receptors for hormones [126–130]. Hormones thereby induce changes in gene expression, titers of second messengers, neurotransmitter release, and even change neural plasticity [114, 120, 129, 131]. These signaling systems are believed to modulate thresholds that need to be overcome to favor a particular behavior or to initiate its execution. Where and how information about actual environment and internal state converge in the nervous system is largely unknown for most behaviors.

Neuroendocrine control of insect acoustic communication

Adjustment of insect behavior to changing situations requires the extraction of sensory information from the environment, its integration with internal physiological states and the generation of behavioral commands. Neural, neuroendocrinal, and endocrinal signals influence this sensory-to-motor processing on all levels.

Insect hormones

In insects, hormones control metabolism, muscle activity, reproduction, growth and development, tanning, and color change. From a molecular point of view, insects possess three classes of hormones [132–134]: (1) peptide hormones: most insect hormones are small polypeptides under 3000 Da [135, 136]; (2) lipophilic hormones: ecdysteroids and JHs; and (3) biogenic amines: octopamine, dopamine, serotonin. Octopamine acts as systemic stress hormone, similar to adrenaline in vertebrates [137]. Dopamine, serotonin, and octopamine change with an insect’s reproductive state. They are involved in behavioral changes during the life cycle of social insects and have an influence on aggressive behaviors in solitary and eusocial insects [138].

Hormonal actions in insects are complex. Like vertebrates, insects possess a blood (or hemolymph) brain barrier. The perineurium, a sheath of specialized glia, encloses the nervous system (CNS and large nerves) and separates it from the circulating hemolymph [139]. While the hemolymph composition underlies fluctuations in chemical composition and ionic concentrations, the perineum enables a constant fluid composition inside the nervous system and also controls the access of hormones to the brain [140].

Hormonal effects on the central nervous system are determined by the receptor types at the target sites and signal transduction pathways within the target cells [113]. More than 45 neuropeptide, peptide, and protein hormone G-protein coupled receptors (GPCRs) have been identified in Drosophila [141]. Hormones may directly act on target tissues or affect the release of other hormones. An example for a hormone with tropic effect is prothoracicotropic hormone (PTTH) which stimulates ecdysteroid release [142]. While hydrophilic hormones bind to receptors located in the cell membrane of their target cells, most lipophilic signaling molecules pass the cellular membranes of their target cells and activate cytosolic or nuclear receptors that regulate gene transcription. Lipophilic hormones may also activate peripheral membrane receptors that mediate physiological effects independent of gene regulation [143,144].

Peptide hormones and biogenic amines typically activate GPCRs within the cellular membrane of target cells and initialize second messenger cascades [145]. Long-term effects by gene regulation are mediated by cAMP/CREB interaction [145]. One of the best studied examples for insect peptide hormones are adipokinetic hormones (AKHs). They mobilize either lipids or carbohydrates from fat body cells and thereby play an important role in energy homoeostasis. Binding of AKHs to their GPCRs leads to an increase of intracellular cAMP levels, release of Ca²  + from intracellular stores, activates the ERK1/2 pathway, and stimulates MAP kinase activity [146–149].

Both PTTH and insulin-like hormones bind to tyrosine kinase receptors [150]. Binding of PTTH to its receptor in prothoracic gland cells activates the ERK pathway and leads to the generation of alpha-ecdysone by controlling the transcription of genes for steroidogenic enzymes (reviewed in Ref. [151]). Alpha-ecdysone produced by the prothoracic gland cells is then converted into its active form 20-hydroxyecdysone, the most common molting hormone in insects [152, 153].

Due to their lipophilic character, ecdysone and JHs are released into the hemolymph immediately after synthesis. While JH is carried to its target sites by binding proteins [154–156], ecdysone is transported freely in the hemolymph [157]. JHs bind to intracellular receptors that interact with gene-regulatory sequences (mostly modulating ecdysone-induced effects) to regulate molting/development. In adult insects JH affects sexual maturation and behavior probably independent of ecdysone. Also membrane bound GPCRs exist for JHs. The nature of the main JH-receptor was long unresolved. Only in 2015, 80 years after the first evidence for JH [158], the bHLH-PAS protein methoprene-tolerant, discovered in 1998 [159, 160] could be genetically confirmed as a JH receptor and the signaling pathway decoded [144,161].

Structure and function of insect neuroendocrine systems

Peptide hormones are released by neurosecretory cells (NSCs). Within the central nervous system, NSCs can not only be found predominantly in the Pars intercerebralis (PI) and Pars lateralis (PL) of the protocerebrum [162, 163] but also the ventral nerve cord contains NSCs releasing, for example, crustacean cardioactive peptide and proctolin [164, 165]. Intrinsic cells of the PI/PL-region release peptide hormones directly into the hemolymph. Other cells from these groups send axonal projections to the neurohemal organs of the retrocerebral complex (or ring gland in Drosophila) [166]. Due to their developmental origin and function, the PI/PL-region has been compared to the hypothalamus in vertebrates [167, 168].

The retrocerebral complex consists of corpora cardiaca (CC), corpora allata (CA), and in diptera also the prothoracic gland [169]. PL and PI innervate the CC by the nervi corporis cardiaci I–III (NCC I–III). The CA are connected to the CC by the nervi corporis allati I (NCA I) and to the subesophageal ganglion by NCA II [170, 171]. The CC not only consists of a storage and a glandular lobe, receives endings of neurosecretory axons but also contains intrinsic secretory cells producing amongst others adipokinetic hormone [172] (Fig. 3).

Fig. 3

Fig. 3 Major components of insect neuroendocrine systems. Neurosecretory cells (purple) in the pars lateralis (PL) and pars intercerebralis (PI) of the brain and in the subesophageal ganglion (SEG) innervate the retrocerebral complex, consisting of the corpora cardiaca (CC) and the corpora allata (CA). NCA , Nervus corporis allati; NCC , nervus corporis cardiaci. Intrinsic neurosecretory cells in the glandular part of the CC ( purple ) secrete adipokinetic hormone (AKH) which mobilizes either lipids or carbohydrates from fat body cells. PTTH is produced by neurosecretory cells in the brain, released by the CA and activates ecdysone production in the prothoracic gland. Juvenile hormone (JH) is produced by the CA and released into the circulation. Ecdysone and JH regulate development, reproductive maturation and neural control of adult reproductive behaviors.

In addition to neurosecretory cells in the central nervous system, endocrine cells exist in the midgut epithelium. They release their content (peptides such as FMRF amide and tachykinins) by exocytosis into the hemolymph [173].

Ecdysone is produced by prothoracic glands, gonads and accessory glands in adult insects. JHs are produced in and released by the CA [11]. Biogenic amines are released by varicose peripheral nerves at diffuse neurohemal-releasing sites [174].

Neuroendocrine regulation of insect acoustic communication—Some well-studied examples

In insects, acoustic communication is part of a manifold behavioral repertoire displayed in certain situations of aggression or mate finding. Studies on various acoustically communicating insects indicated that both the production of acoustic signals and the behavioral responses initiated by these are largely regulated by three different mechanisms that act on different time scales.

Hormones act as regulators of phenotypic plasticity through establishment or reconfiguration of neural circuits that are essential for sound production and acoustically guided behavior. They determine developmental, social, and reproductive states which are associated with sound production in general, particular signals and state-dependent behavioral responses.

Neuromodulators regulate the release-threshold for acoustic communication, thereby biasing an insect’s motivation to favor appropriate behaviors (including particular acoustic signals and specific responses to them) in a particular situation. Conditions that favor or disfavor acoustic signal production (e.g., illumination, ambient noise, temperature, being restrained in an experiment) may, via release of neuromodulators, differentially alter the impact of sensory input making a particular acoustic behavior more or less likely and/or more or less intensely executed.

Transmitters, released within decision-making premotor regions of the central nervous system trigger the production of acoustic signals and immediate reactions induced by their perception.

One example with knowledge about neuroendrocrinal signals acting on all three levels is the song production of female Chorthippus biguttulus grasshoppers [175]. A particular level of JH released from the corpora allata reflects the reproductive state of an individual female and represents a prerequisite for song production, typically stimulated by male calling or courtship songs. Release of nitric oxide in the central complex (e.g., when grasshoppers are restrained during an experiment) mediates (indirect) inhibition of stridulatory command neurons, thereby increasing the threshold for sound production. Release of acetylcholine in the central complex (e.g., following perception of a male’s calling song) excites stridulatory command neurons that invariantly activate thoracic pattern generators to produce a song sequence.

More details on the regulation of grasshoppers’ acoustic behaviors and other acoustically communicating insects will be summarized in the following.

Grasshoppers

Acoustically communicating grasshoppers typically generate sound signals by hind leg-against-forewing stridulation. Neuromuscular excitation patterns underlying rhythmic movements of the hind legs are generated by hemiganglionic circuits located in the metathoracic ganglion complex [49, 51, 176]. Some species generate distinct calling, courtship, and aggression songs but knowledge about the synaptic connectivity of pattern generating interneurons, their transmitters and the convergence of different output patterns on the motorneurons that innervate the hind leg muscles is essentially lacking. Three different types of command neurons that connect the brain with the thoracic pattern-generating circuits have been identified in the species Omocestus viridulus. Each command neuron is sufficient to activate one of three different patterns of hind leg movements and resulting sounds involved in calling and courtship singing [50, 82]. In contrast, no command neuron that initiates aggression song was found to date.

Stridulatory command neurons are activated (either directly or indirectly) by output neurons of the central complex (Fig. 4). This prominent brain neuropil has been demonstrated to regulate grasshopper sound production with respect to pattern selection, temporal structure, and intensity of calling and courtship songs [51, 177]. The central complex receives multimodal sensory input that is processed and integrated through a large number of different transmitters and neuromodulators (reviewed by Ref. [178]). Transmitters and neuromodulators involved in the control of sound production by the central complex have been identified in the grasshopper species C. biguttulus, for which a large body of data on acoustic behaviors (male and female sound production, sound perception, and information processing) exists. Recognition of calling song (by females) or female song (by males) mediates the release of ACh that excites columnar output neurons of the central complex via nicotinic and muscarinic receptors, the latter leading to an accumulation of cyclic AMP upon repetitive excitation which lowers the threshold to initiate a response song [179–181]. In addition to ACh, focal application of proctolin and dopamine to the central complex also stimulates sound production, though specific sensory stimuli leading to their release have not been determined. Disturbing stimuli, such as noise or light flashes, terminate ongoing sound production (or prevent its initiation) by release of GABA leading to direct inhibition of the columnar (stridulation-promoting) central complex neurons [181]. Situations, in which sound production is inappropriate, like being handled by an experimenter or being restrained during an experiment, elicit the release of the gaseous transmitter nitric oxide from pontine and tangential neurons in the upper division of the central complex. This indirectly inhibits the columnar neurons through activation of GABAergic terminals that synapse on these in the lower division [175, 181, 182]. Short-term regulation of sound production seems to rely on a balance of excitatory and inhibitory synaptic input to columnar output neurons of the central complex, which reflect sensory stimuli that promote or suppress sound production.

Fig. 4

Fig. 4 Neuronal control of sound production and perception in acridid grasshoppers. (A) Schematic of the central nervous system with brain, subesophageal ganglion (SEG) and the three thoracic ganglia (T1–3). Auditory pathways are depicted in orange and red , motoric pathways for sound production are depicted in blue . Axons of auditory receptor neurons in the ear enter the metathoracic ganglion complex (T3) through the auditory nerve and terminate in the primary auditory neuropil. Here, local interneurons process auditory input and relay the information to ascending interneurons. Recognition of (conspecific) acoustic patterns is achieved by auditory neuropils in the lower lateral protocerebrum (LL). The central complex integrates processed sensory information relevant to sound production and activates (either directly or indirectly) command neurons that connect to the central pattern generators within T3. These circuits generate the neuromuscular excitation patterns underlying song production by stridulatory hind leg movements. CB , Central body; MB , Mushroom body. (B) Position of ear and central nervous system (light blue) in a locust. Scale bars: 5 mm.

Additionally, the physiological state seems to influence reproduction-related acoustic behaviors on a longer time scale. Sexual maturation and previous mating experience influence reproductive readiness in both sexes [175, 183]. Female reproductive readiness critically depends on JH, an important regulator of insect development [184] and reproductive maturation [153]. JH is released into the hemolymph by parenchymal cells of the corpora allata and acts on cellular targets in the ovaries, the nervous system, and probably diverse other tissues. Direct influence on reproductive behaviors has been demonstrated in various insects, including acoustically communicating grasshoppers [185]. Relatively high levels of JH are required around the time of imaginal molt to induce reproductive readiness associated with active song production at 6–7 days of age. If JH signaling is prevented in young females, reproductive behaviors, including song production, will be prevented throughout lifetime [175]. By contrast, mature females seem to require low levels of JH to maintain reproductive readiness. Both mating and oviposition have been shown to alter JH titers in grasshopper (and other insect) females, leading to inhibition of spontaneous song production, suppression of responses to male calling songs and hence rejection of any male mating attempts [175]. How the general reproductive state, partly represented by JH, determines whether appropriate sensory input can initiate grasshopper song production is not clear to date. JH may directly (or indirectly by triggering the release of other hormones) alter the sensitivity to and processing of acoustic signals and other sensory input related to social interactions, thereby limiting or enabling acoustic behaviors (an example in Drosophila melanogaster is discussed below). Alternatively, direct neural information flow between brain and corpora allata could establish coherent activities of endocrinal and neural systems to foster particular behaviors. Anatomical studies in C. biguttulus revealed brain neurons (in pars intercerebralis and pars lateralis) and neurons in the corpora allata that establish mutual connections between these regions and a bidirectional information flow, modulated by oviposition cycles, was observed in migratory locusts (unpublished data). However, where and how hormonal signals representing the reproductive state are integrated with neural processing of sensory information concerned with reproduction-related sound production requires further studies.

Crickets

Various crickets generate distinct calling-, courtship-, and aggression songs by rhythmically rubbing their forewings (elytra) against each other. The underlying neuromuscular excitation patterns are generated by neuronal circuits in the metathoracic ganglion complex, the first free abdominal ganglion and the wing muscle motorneurons in the mesothoracic ganglion [186, 187]. Studies on Gryllus bimaculatus identified one bilateral pair of command neurons that stimulate both calling and courtship songs [188] (Fig. 5). Focal injections of cholinergic agonists to their dendritic regions in the brain elicited stridulatory activity switching between calling and courtship patterns at some stimulation sites and between calling and aggression patterns at others [189]. This suggests that, in addition to descending commands from the brain, other mechanisms contribute to the selection of song type according to the situation encountered. Similar factors that promote calling- and courtship song production in grasshoppers (illumination, ambient noise, presence of females, and others, discussed earlier) also stimulate cricket calling and courtship behavior. In addition, the neuro-endocrinal regulation of male crickets’ aggressive behaviors, that include aggression songs, has been intensely studied. Male crickets compete for territories that provide shelter, food, and attraction of females. Aggression songs are typically performed after bouts of fighting (by both contestants) and after the winner and loser have been determined (only by the winner) [190, 191]. These songs have been identified as an important signal to promote the surrender of one opponent [192]. Several transmitters, neuromodulators, and hormones have been linked to enhanced aggression as a consequence of winning a fight and reduced aggression (essentially avoidance of aggressive interactions) as a consequence of defeat. The decision to surrender and retreat from fighting is ultimately triggered by the release of nitric oxide in the brain [193] and experimental suppression of nitric oxide formation during fights prevents subsequent states of reduced aggression and conflict avoidance which are mediated by serotonin [194]. In contrast, both dopamine and octopamine seem to enhance male cricket aggression and/or re-establish aggressive motivation of defeated crickets [117,194–196]. How these signals impact the generation of aggressive song, either by direct effects on the command neurons or the central pattern generators or other indirect mechanisms, remains to be studied.

Fig. 5

Fig. 5 Neuronal control of sound production and perception in crickets. (A) Scheme of the central nervous system with brain, subesophageal ganglion (SEG), three thoracic ganglia (T1–3, T3 fused with the first two abdominal ganglia A1–2), and the abdominal ganglion (A3). Auditory pathways are depicted in orange and red , motoric pathways for sound production are depicted in blue . Axons of auditory receptor neurons enter the prothoracic ganglion and terminate in the primary auditory neuropil. Local auditory interneurons process auditory information and relay it to ascending interneurons that transmit the preprocessed information to higher order auditory neuropils in the brain. Production of calling and courtship songs is initiated by descending command neurons that activate central pattern generators (CPGs) in T3-A2 and A3. These circuits generate the characteristic excitation patterns for song production and activate the motor neurons in T2 controlling the movement of the fore wings during stridulation. CB , Central body; MB , Mushroom body. (B) Position of ear and central nervous system (light blue) in a field cricket. Scale bars: 5 mm.

Honeybees

Honeybee colonies consist of a reproductively active queen, some male drones and a huge number of workers that perform different age-related tasks. During the first 2–3 weeks of their adult life, workers serve as nurse bees involved in brood care, followed by a few days with different in-hive tasks (e.g., building honeycomb cells, storing food, guarding hive entrance) and another 1–2 weeks as foragers collecting nectar and pollen [197, 198]. Functional organization of a honeybee colony in a dark hive relies on chemical and vibroacoustic communication between its individuals. Both workers and queens produce different task-related vibroacoustic signals, typically by wing muscle-generated oscillations of the thorax that give rise to near-field air-borne sounds, substrate vibrations or contact-mediated vibration of nest mates with fundamental frequencies ranging from 300 to 600 Hz [199–201]. The types of vibroacoustic patterns produced by an individual honeybee may quickly switch. Young queens that are still confined in their brood cells produce quacking sounds to inform other young queens and nurse bees about their presence. Right after emergence from brood cells, they switch to tooting sounds. The interplay of tooting and quacking is thought to regulate the number of new queens emerging from brood cells and the competition between the young queens [199, 202, 203]. Vibroacoustic signals may signal general states of activity to nest mates [204] and represent essential parts of particular worker behaviors intended to activate the colony, alarm nest mates, recruit other workers to particular tasks and provide information about locations of food sources [201]. Since the age-related assignment to different tasks can be accelerated, slowed down, or even reverted (e.g., by changing the composition or predominant needs of the colony [205]), workers seem to be capable of producing the complete repertoire of sound signals throughout their adult life but only activate those signals that are associated with their actual task and/or physiological state. How this is regulated, and in particular which ultimate trigger releases sound production, has not been elucidated in detail. However, multiple factors that regulate the age- and condition-related division of labor (including JH, octopamine, vitellogenin, and insulin-like peptides) [206, 207] and brain regions relevant for the control of state-specific tasks including sound production (Mushroom bodies, antennal lobes, and subesophageal ganglion) have been determined. Likely, the same chemical messengers and brain regions also regulate the processing of information leading to the generation of vibroacoustic signals that accompany particular worker behaviors.

Fruit flies

The fruit fly D. melanogaster represents the actually most intensely studied insect species, due to easy generation of mutant strains and the availability of research tools that allow precise genetic interference with the expression of particular genes in particular cells at particular times. Acoustic signals generated by wing vibrations and perceived by Johnston’s organs located in the antennae are essential components of male courtship and intermale competition [29, 208, 209]. Auditory sensory neurons relay their information to the antennal mechanosensory and motor center (AMMC) zones in the brain. Giant fiber neurons convey information to the thoracic ganglion where direct and indirect flight muscles are activated [58, 208, 210] (Fig. 6). Exposure to courtship or aggression songs has been shown to promote male Drosophila to perform or intensify the respective behavior [211, 212]. Biogenic amines have been demonstrated to bias the execution of either courtship or aggression (octopamine promotes aggression [213]). They modulate aggression with respect to previous fighting experience and other physiological parameters such as nutritional state (dopamine, serotonin, octopamine, tachykinins, and insulin-like peptides; reviewed by Refs. [214, 215]). Courtship is modulated with respect to recent activity, age, and physiological state (dopamine [216, 217] and the levels of circulating JH [218]). However, transmitters and neuromodulators may affect behaviors associated with acoustic signal production at particular sites within the respective neural circuits and/or via neurons that express a particular type of receptor and these local effects might differ from global upregulation or downregulation of their neuromodulatory impact. While only male D. melanogaster naturally generate courtship songs (other species such as D. virilis perform bidirectional acoustic communication [219]), females seem to contain the full circuitry required to generate both sine- and pulse-patterns of the male courtship song [53, 220, 221]. Reduction of ecdysteroid signaling (produced in adult flies’ ovaries) or knockdown of cytosolic ecdysteroid receptor in neurons that express the sex-specific transcription factor fruitless enabled females to perform both song patterns during interactions with conspecifics [222]. Song production of D. melanogaster females therefore seems to be prevented by weak coupling of courtship-promoting sensory input and/or reduced excitability [221] of song-initiation circuits, which is at least partly mediated by hormonal influence. Another hormone, JH released from the corpora allata, increases courtship activity including courtship song production in older compared with younger males. JH, via activating its putative receptor methoprene-tolerant, sensitizes odorant receptors for the pheromone palmitoleic acid leading to a stronger representation of this courtship-stimulating cue and hence more intense courtship [218]. Increasing knowledge about the neural circuits involved in acoustic signal processing and sound production will link particular acoustic (and other) signals to activation of particular neurons and determine the impact of locally released transmitters and neuromodulators in connection with globally acting circulating hormones on the performance of courtship and aggression including their acoustic components.

Fig. 6

Fig. 6 Neuronal control of sound production and perception in fruit flies. (A) Schematic of the central nervous system with brain, subesophageal ganglion (SEG), and fused thoracoabdominal ganglion complex (TG). Auditory pathways are depicted in orange , motoric pathways for sound production are depicted in blue . Acoustic signals are perceived through Johnston’s organs located in the antennae. Auditory sensory neurons relay their information to the antennal mechanosensory and motor center (AMMC) zones in the brain. Giant fiber neurons (GF) convey information to the thoracic ganglion where direct and indirect