Animals exhibit extraordinary variation in their behavior, yet little is known about the neural mechanisms that generate this diversity. My lab has been taking advantage of the rapid diversification of male courtship behaviors in Drosophila to glean insight into how evolution shapes the nervous system to generate species-specific behaviors. By translating neurogenetic tools from D. melanogaster to closely related Drosophila species, we have begun to directly compare the homologous neural circuits and pinpoint sites of adaptive change. Across species, P1 neurons serve as a conserved node in regulating male courtship: these neurons are selectively activated by the sensory cues indicative of an appropriate mate and their activation triggers enduring courtship displays. We have been examining how different sensory pathways converge onto P1 neurons to regulate a male’s state of arousal, honing his pursuit of a prospective partner. Moreover, by performing cross-species comparison of these circuits, we have begun to gain insight into how reweighting of sensory inputs to P1 neurons underlies species-specific mate recognition. Our results suggest how variation at flexible nodes within the nervous system can serve as a substrate for behavioral evolution, shedding light on the types of changes that are possible and preferable within brain circuits.

How does the brain decode the meaning of sound signals, such as music and courtship songs? We believe that the fruit fly Drosophila melanogaster is an ideal model for answering this question, as it offers a comprehensive range of tools and assays which allow us to dissect the mechanisms underlying sound perception and evaluation in the brain. During the courtship behavior, male fruit flies emit “courtship songs” by vibrating their wings. Interestingly, the fly song has a species-specific rhythm, which indeed increases the female’s receptivity for copulation as well as male’s courtship behavior itself. How song signals, especially the species-specific sound rhythm, are evaluated in the fly brain? To tackle this question, we are exploring the features of the fly auditory system systematically. In this lecture, I will talk about our recent findings on the neural basis for song evaluation in fruit flies.

For many animals, the sense of olfaction plays a major role in controlling sexual behaviors. Olfaction helps animals to detect mates, discriminate their status, and ultimately, decide on their behavioral output such as courtship behavior or aggression. Specific pheromone cues and receptors have provided a useful model to study how sensory inputs are converted into certain behavioral outputs. With the aid of recent advances in tools to record and manipulate genetically defined neurons, our understanding of the neural basis of sexual and social behavior has expanded substantially. I will discuss the current understanding of the neural processing of sex pheromones and the neural circuitry which controls sexual and social behaviors and ultimately reproduction, by focusing on rodent studies, mainly in mice, and the vomeronasal sensory system.

Animals produce behavior by responding to a mixture of cues that arise both externally (sensory) and internally (neural dynamics and states). These cues are continuously produced and can be combined in different ways depending on the needs of the animal. However, the integration of these external and internal cues remains difficult to understand in natural behaviors. To address this gap, we have developed an unsupervised method to identify internal states from behavioral data, and have applied it to the study of a dynamic social interaction. During courtship, Drosophila melanogaster males pattern their songs using cues from their partner. This sensory-driven behavior dynamically modulates courtship directed at their partner. We use our unsupervised method to identify how the animal integrates sensory information into distinct underlying states. We then use this to identify the role of courtship neurons in either integrating incoming information or directing the production of the song, roles that were previously hidden. Our results reveal how animals compose behavior from previously unidentified internal states, a necessary step for quantitative descriptions of animal behavior that link environmental cues, internal needs, neuronal activity, and motor outputs.

During communication, alignment between signals and sensors can be critical. Signals are often best perceived from specific angles, and sensory systems can also exhibit strong directional biases. However, we know little about how animals establish and maintain such signaling alignment during communication. To investigate this, we characterized the spatial dynamics of visual courtship signal- ing in the jumping spider Habronattus pyrrithrix. The male performs forward-facing displays involving complex color and movement patterns, with distinct long- and short-range phases. The female views displays with 2 distinct eye types and can only perceive colors and fine patterns of male displays when they are presented in her frontal field of view. Whether and how courtship interactions pro- duce such alignment between male display and female field of view is unknown. We recorded relative positions and orientations of both actors throughout courtship and established the role of each sex in maintaining signaling alignment. Males always oriented their displays toward the female. However, when females were free to move, male displays were consistently aligned with female princi- pal eyes only during short-range courtship. When female position was fixed, signaling alignment consistently occurred during both phases, suggesting that female movement reduces communication efficacy. When female models were experimentally rotated to face away during courtship, males rarely repositioned themselves to re-align their display. However, males were more likely to present cer- tain display elements after females turned to face them. Thus, although signaling alignment is a function of both sexes, males appear to rely on female behavior for effective communication

For social animals, successfully communicating with others is essential for interactions and survival. My research aims to answer a central question on the neuronal basis of this ability, from the perspective of the listener: how do our brains enable us to communicate with each other? My work develops nonhuman animal models to study the behavioural and neuronal mechanisms underlying the perception of vocal patterns. I will start by providing an overview of my past research characterizing the neuronal-level substrates of voice processing along the primate temporal lobe. I will then focus on my current work on vocal perception in mice, in which I utilize natural male-female courtship behaviour to evaluate the acoustic dimensions extracted by listeners from ultrasonic sequences. I will then talk about ongoing work investigating the neuronal substrates supporting the perception of behaviourally relevant acoustic cues from mouse vocal sequences.

Courtship behavior is an innate model for many types of brain computations including sensory detection, learning and memory, and internal state modulation. Despite the robustness of the behavior, we have little understanding of the underlying neural circuits and mechanisms. The Stowers’ lab is leveraging the ability of specialized olfactory cues, pheromones, to specifically activate and therefore identify and study courtship circuits in the mouse. We are interested in identifying general circuit principles (specific brain nodes and information flow) that are common to all individuals, in order to additionally study how experience, gender, age, and internal state modulate and personalize behavior. We are solving two parallel sensory to motor courtship circuits, that promote social vocal calling and scent marking, to study information processing of behavior as a complete unit instead of restricting focus to a single brain region. We expect comparing and contrasting the coding logic of two courtship motor behaviors will begin to shed light on general principles of how the brain senses context, weighs experience and responds to internal state to ultimately decide appropriate action.

Attending to mistakes while practicing alone provides opportunities for learning but self-evaluation during audience-directed performance could distract from ongoing execution. It remains unknown how animals switch between practice and performance modes, and how evaluation systems process errors across distinct performance contexts. We recorded from striatal-projecting dopamine (DA) neurons as male songbirds transitioned from singing alone to singing female-directed courtship song. In the presence of the female, singing-related performance error signals were reduced or gated off and DA neurons were instead phasically activated by female vocalizations. Mesostriatal DA neurons can thus dynamically change their tuning with changes in social context.

Many innate behaviours are the result of multiple sensorimotor programs that are dynamically coordinated to produce higher-order behaviours such as courtship or architecture construction. Extendend phenotypes such as architecture are especially useful for ethological study because the structure itself is a physical record of behavioural intent. A particularly elegant and easily quantifiable structure is the spider orb-web. The geometric symmetry and regularity of these webs have long generated interest in their behavioural origin. However, quantitative analyses of this behaviour have been sparse due to the difficulty of recording web-making in real-time. To address this, we have developed a novel assay enabling real-time, high-resolution tracking of limb movements and web structure produced by the hackled orb-weaver Uloborus diversus. With its small brain size of approximately 100,000 neurons, the spider U. diversus offers a tractable model organism for the study of complex behaviours. Using deep learning frameworks for limb tracking, and unsupervised behavioural clustering methods, we have developed an atlas of stereotyped movement motifs and are investigating the behavioural state transitions of which the geometry of the web is an emergent property. In addition to tracking limb movements, we have developed algorithms to track the web’s dynamic graph structure. We aim to model the relationship between the spider’s sensory experience on the web and its motor decisions, thereby identifying the sensory and internal states contributing to this sensorimotor transformation. Parallel efforts in our group are establishing 2-photon in vivo calcium imaging protocols in this spider, eventually facilitating a search for neural correlates underlying the internal and sensory state variables identified by our behavioural models. In addition, we have assembled a genome, and are developing genetic perturbation methods to investigate the genetic underpinnings of orb-weaving behaviour. Together, we aim to understand how complex innate behaviours are coordinated by underlying neuronal and genetic mechanisms.

Animals exhibit extraordinary variation in their behaviour, yet little is known about the neural mechanisms that generate this diversity. My lab has been taking advantage of the rapid diversification of male courtship behaviours in Drosophila to gain insight into how evolution shapes the nervous system to generate species-specific behaviours. By translating neurogenetic tools from D. melanogaster to closely related Drosophila species, we have begun to directly compare the homologous neural circuits and pinpoint sites of adaptive change. Across species, P1 interneurons serve as a conserved and key node in regulating male courtship: these neurons are selectively activated by the sensory cues carried by an appropriate mate and their activation triggers enduring courtship displays. We have been examining how different sensory pathways converge onto P1 neurons to regulate a male’s state of arousal, honing his pursuit of a prospective partner. Moreover, by performing cross-species comparison of these circuits, we have begun to gain insight into how reweighting of sensory inputs to P1 neurons underlies species-specific mate recognition. Our results suggest how variation at flexible nodes within the nervous system can serve as a substrate for behavioural evolution, shedding light on the types of changes that are possible and preferable within brain circuits.