Philip K. Stoddard - US grants

Neuroscientists rely on animal models for the investigation of basic neural processes. Within this broad field, neuroethology has focused on the analysis of natural behaviors, often those associated with sensory processing of critical signals. Our understanding of the neuroanatomy, physiology, and development of human sensory systems comes largely from study of vertebrate model system. Glymnotiform electric fish have become leading models for investigation of parallel processing and organization among neural networks in vertebrate sensory and motor systems. Neuroscientists have traced the electrosensory pathway from the sensory periphery, through the brain, and back to the motor output. Gymnotiform electric fish use the same neural networks for three different functions: electrolocation, communication, and jamming avoidance. The gymnotiform electrosensory system is therefore an excellent model for exploring the flexibility of parallel processing networks. Behavioral studies of these three sensory functions form the base for investigation of the properties of the brain networks involved. This study is designed to reveal the behavioral mechanism(s) of electric signal discrimination involved in social communication. Further investigation of underlying networks and neural mechanisms can follow once we know the behavioral algorithms that electric fish use to discriminate among signal waveforms. Gymnotiform fish appear to control their motor output (electric signals) to enhance their sensory processing of signals from other fish. Combined signals sum to overcome inertia of the peripheral receptor system but must be separated once again by the central networks. The study proposed here follows a rational progression. 1. A calibrated set of natural signals will be digitized from the fish in an outdoor breeding colony for use as stimuli in subsequent experiments. 2. The next step will be to calibrate the sensory thresholds of the study species by obtaining two types of behavioral tuning curves: sensitivity to pure signals and the sensitivity to combined signals of receiver and signaler. 3. Signal motor patterns will be recorded in experiments that elicit natural discrimination behavior. Motor behavior in this context will be subjected to detailed analysis to document precisely when and how the receiver overlaps its signal with that of the signaler (i.e., combines signals). 4. The final experiments in this proposal will reveal the salient features used for signal discrimination and the motor behaviors required for accurate discrimination of signals.

We have developed a model system for exploring how changes in an animal's physical and social environment result in the remodeling of its excitable membranes. The teleost electric fish Brachyhypomus pinnicaudatus produces an electric waveform for electrolocation and communication. Shape and amplitude of the electric waveform are determined by ion conductance and kinetics of excitable membranes in the electric organ. Waveform properties change both gradually (hours- days) and quickly (minutes). These two time courses are consistent with genomic steroid action and a non-genomic action respectively of unidentified hormones working to modify the excitable membranes of the electric organ. We can elicit changes in the fish's electric waveform properties by manipulating light and social conditions in the lab. In the project proposed, we shall determine which hormones produce the rapid and slow changes we see in the electric waveform and identify the ionic mechanisms underlying the changing waveform. A strength of this system is the scope of its biological relevance; we understand the behavioral significance of the electric waveform changes, so by determining the cellular and molecular mechanisms, we can draw a long chain of continuous causal connections, from social behavior to the underlying gene regulation of ion channels and 2nd messenger systems. A potential benefit of this project is the possibility of localizing important new biomolecules including membrane receptors for sex steroids.

Circadian rhythms are often disrupted with advancing age and under conditions of stress, including social stress. Breakdown in human circadian rhythms are believed to occur most often downstream of the central circadian oscillator. Our lab has developed electric fish as a powerful non-mammalian vertebrate model system in which controlled changes in the social environment alter predictably the magnitude of two circadian rhythms in electric signal waveform parameters. Our system makes a valuable model because we have identified multiple social conditions that modulate circadian rhythm expression in multiple ways. As with mammalian models, situations promising social upheaval disrupt the circadian outputs. Social isolation, however, causes a progressive diminution of these rhythms, as though the coupling between the central oscillator and the peripheral effector had been weakened or broken. Restoration of favorable social conditions restores the strength of the rhythms. We have made significant progress in identifying the neurochemical components of the circadian output pathway. Two neurochemical messengers, 5-HT and ACTH, modulate the behavioral outputs, ACTH at the level of the peripheral effector organ. Results with males indicate that the circadian rhythms are regulated somewhere downstream of serotonin. We also have found that non-aromatizable androgens can enhance the amplitude of these circadian rhythms in a manner resembling certain favorable social manipulations. Building on our progress to date, we propose specific aims (1) to better understand the behavioral conditions that regulate circadian rhythms in the electric waveform, (2) to elucidate the roles of androgens and glucocorticoids in regulating the circadian rhythms, and (3) to identify which hormones of the hypothalamus-pituitary-adrenal axis are in direct control of the circadian outputs. Because the neuroanatomy and neurochemistry of the circadian control pathway have been conserved across vertebrate evolution, these studies will lead directly to testable hypotheses about mechanisms !underlying circadian rhythm pathologies in mammals, including humans.

Dishonest communication is widespread throughout in the animal kingdom, including humans, but mechanisms that produce dishonest signals are poorly understood. Likewise, researchers do not clearly understand how honest and dishonest communication coexists stably in communication systems, including our own. The central question in this study is how dishonesty alters the meaning of communication signals. To address this question, the project focuses on (i) how signal dishonesty and the physiological costs of signaling alter the reliability and meaning of communication signals, and (ii) how listeners assess the quality of signalers who inaccurately convey their particular qualities. This project investigates signal exaggeration by electric fish, an ideal model system because their signals can be quantified with unusual accuracy and manipulated pharmacologically. Methods will include electrophysiology, measurement of energetic output, endocrinology, and behavioral experiments. This project (1) quantifies three mechanisms that signalers use to control signal strength, (2) determines the behavioral meaning and reliability of signal strength under different social contexts, (3) determines how receivers assess and use information that has been altered by exaggeration, and (4) uses this information to address and revise theory of how communication systems can persist in the face of dishonesty and unreliability. The resources of this research project will be used to foster science education. This goal will be approached by assisting middle-school science teachers in devising a more engaging hands-on curriculum and by providing opportunities for direct mentorship of minority college and high school students.

Successful communication and social assessment require receivers to discern when signals are reliable and when they are not. Compounding the problem is that signal reliability varies between signalers and across time within signalers. Because communication systems are not intrinsically reliable, primates, especially humans, spend a great deal of time and resources assessing the reliability of information received from members of their own species. Surprisingly, hard-wired communication systems of animals with simpler communication systems than humans are proving no more reliable, and we do not know how receivers in these species deal with unreliability of signals. This project will focus on a species with less sophisticated cognition to examine how fundamental strategies have evolved to cope with unreliable signals, the most important outstanding scientific puzzle in the field of communication. The investigator will also continue a successful hands-on science pedagogy workshop series that brings inquiry-based teaching methods into middle school classrooms, as well as offering direct mentorship opportunities for minority college and high school students in the research lab.

The proposed project will address the central question by determining (1) whether receivers know when signals are reliable and when they are not, (2) whether receivers have strategies for addressing variable reliability and (3) whether signalers compensate for a receiver's lack of trust by providing more reliable information through other means. Male electric fish (Brachyhypopomus gauderio) are ideal for such investigation because their signal waveforms encode body length and androgen level with near perfect reliability, or virtually no reliability. Signal reliability in this system depends on population density and food availability. These variables will be controlled in the lab to promote reliable and unreliable signals, and to create prior exposure of receivers to signals that vary in reliability. Behavioral mate choice and male-male competition experiments will determine whether receivers assess reliability of a male signal by (i) monitoring prevailing social and food conditions, (ii) reviewing recent signal reliability, or (iii) whether receivers ignore signals and assess other, more reliable traits. The project will also determine whether signalers compensate for their lack of reliability by making the desired information readily available through other sensory strategies. Both raw and analyzed data are secured by the investigator prior to publication and made available for electronic sharing upon acceptance of the resulting manuscripts.