Jan Clemens

Communication signals often contain behaviorally relevant structure on multiple temporal scales. Short-timescale features are commonly thought to be recognized first and then integrated into longer-timescale representations. Whether a shared circuit can instead recognize multiple timescales remains unclear. Cricket calling songs provide a tractable test because millisecond-scale pulses are grouped into chirps lasting hundreds of milliseconds. We combined female phonotaxis with a mechanistic model of the identified pulse-recognition network to ask whether this circuitry can also generate chirp selectivity. In Gryllus bimaculatus , the model, originally parameterized from pulse-scale electrophysiology and behavior, recovered the main boundaries of chirp preference without fitting to chirp behavior. Coincidence detection generated the minimum chirp-duration requirement, whereas suppressive computations in the network’s input neuron shaped the upper boundaries for chirp duty cycle and period. Across 14 species, varying these suppressive computations captured major differences in chirp tuning. These findings reveal a temporally interleaved serial circuit in which long-timescale selectivity begins upstream of completed short-timescale selectivity, offering an alternative to both conventional short-first hierarchies and parallel pathways.

Male Drosophila courtship includes two communication signals: airborne song and substrate-borne vibrations. While the neural control of song has been extensively characterized, little is known about the circuits underlying vibration production. Here, we identify neurons expressing the Hox gene abdominal-B ( abdB ) as a driver of vibration production. Optogenetic activation of abdB neurons selectively elicited vibrations in both males and females without inducing courtship song, whereas silencing these neurons did not impair vibration production during natural courtship. The vibration-driving abdB neurons are neither doublesex -nor fruitless -positive, defining a previously unrecognized component of the courtship circuit. Although abdB activation produced only stimulus-locked vibrations, co-activation of the persistence-promoting neuron cluster pCd converted this transient signal output into sustained vibration trains. Together, our results identify a dedicated pathway for vibration production and show that signal identity and persistence can be independently specified by distinct circuit components.

How the brain enables individuals to adapt behavior to their partner is key to understanding social exchange. For example, courtship behavior involves sensorimotor processing of signals that can result in behavioral dialog between partners, such as stereotyped movements and singing. The courtship behavior of Drosophila melanogaster males with their partners, which are usually female but can also be male, involves singing. To investigate how behavioral feedback and sensorimotor processing contribute to flexible social interactions, we compared the courtship behavior and singing of male D. melanogaster towards males and females. Quantitative analysis of their interactions revealed that while underlying courtship and song rules are unaffected by the sex of the partner, the behavioral dynamics and song sequences differ by partner sex. This divergence stems from sex-specific behavioral feedback: females decelerate to song, while males orient towards the singer. Moreover, optogenetic manipulations reveal that the partners’ responses are driven by sex-specific neural circuits that link song detection with arousal and social decisions. Our findings demonstrate that flexible social behaviors can arise from fixed sensorimotor rules through a context-dependent selection facilitated by the partner’s behavioral feedback. More broadly, our results reveal compositionality as a key mechanism for achieving behavioral flexibility during complex social interactions such as courtship.

Many animals produce multimodal displays that combine acoustic, visual, or vibratory signals, yet the neural mechanisms coordinating these behaviors remain unclear. Using Drosophila courtship as a model, we reveal how a single neural circuit integrates sensory cues and motivational state to orchestrate multimodal signaling. Male flies produce both air-borne song and substrate-borne vibrations during courtship, but in distinct, largely non-overlapping contexts. We demonstrate that the same brain neurons that drive song also control vibrations through separate pre-motor pathways, with cell-type specific dynamics. This shared circuit coordinates multimodal displays with locomotion, ensuring vibrations are produced only when they can effectively reach the female. The circuit employs shared motifs—recurrence and mutual inhibition—that enable dynamic control of multimodal signals by external cues and internal state. A computational model confirms that these motifs are sufficient to explain the observed behavioral dynamics. Our findings illustrate how simple neural circuit elements can be combined to select and coordinate complex multimodal behaviors.

Animals need to integrate sensory information from multiple modalities to interact with their environment and with others. In male Drosophila , multiple sensory cues modulate social behaviors such as courtship and aggression, but the strategies by which multimodal cues are combined to inform social behavior are not known. Here, we focus on how courtship song and taste cues are integrated to shape the social behavior of male flies. By combining cue manipulations with computational modeling, we assessed the individual and combined contributions of song and taste. Our results reveal three context-specific integration strategies. Overall social interactions were driven by a linear combination of song and taste. Aggression was driven by song, independent of taste cues. Courtship was controlled by a nonlinear integration of song and female taste cues, with female taste flipping the valence of song from suppressing to enhancing courtship. Our results show how context-specific integration strategies allow animals to recognize social scenarios and produce flexible, context-appropriate behaviors.

Summary: Animals need to fine-control the speed and direction of locomotion to navigate complex and dynamic environments. To achieve this, they integrate multimodal sensory inputs with their internal drive to constantly adjust their motor output. This integration involves the interplay of neuronal populations across different hierarchical levels along the sensorimotor axis – from sensory, central, and modulatory neurons in the brain to descending neurons and motor networks in the nerve cord. Here, we characterize two populations of neurons that control distinct aspects of walking on different hierarchical levels in Drosophila . First, we use in-vivo electrophysiological recordings to demonstrate that moonwalker descending neurons (MDN) integrate antennal touch to drive changes in walking direction from forward to backward. Second, we establish DopaMeander as an important component in the control of forward walking through a combination of optogenetic activation, silencing, connectomics, and in-vivo recordings. These dopaminergic modulatory neurons drive forward walking with increased turning, and the activity of individual neurons is correlated with ipsiversive turning. Hence, MDN and DopaMeander control opposite regimes of walking on different hierarchical levels. Computational models reveal that their activity predicts key parameters of spontaneous walking. Moreover, we find that both MDN and DopaMeander are gated out during flight. This suggests that neuronal populations across levels of control are modulated by the behavioral state to minimize cross-talk between motor programs.

How the brain enables individuals to adapt behavior to their partner is key to understanding social exchange. For example, courtship behavior involves sensorimotor processing of signals that can result in behavioral dialogue between partners, such as stereotyped movements and singing. The courtship behavior of Drosophila melanogaster males with their partners, which are usually female but can also be male, involves singing. To investigate how behavioral feed-back and sensorimotor processing contribute to flexible social interactions, we compared the courtship behavior and singing of male D. melanogaster towards males and females. Quanti-tative analysis of their interactions revealed that while underlying courtship and song rules are unaffected by the sex of the partner, the behavioral dynamics and song sequences differ by partner sex. This divergence stems from sex-specific behavioral feedback: females decelerate to song, while males orient towards the singer. Moreover, optogenetic manipulations reveal that the partners’ responses are driven by sex-specific neural circuits that link song detection with arousal and social decisions. Our findings demonstrate that flexible social behaviors can arise from fixed sensorimotor rules through a context-dependent selection facilitated by the partner’s behavioral feedback. More broadly, our results reveal compositionality as a key mechanism for achieving behavioral flexibility during complex social interactions such as courtship.

Complex vocal communication requires precise, flexible adjustments to vocal-motor commands for the production of coherent responses to auditory inputs. The mechanisms underlying how such sensorimotor integration controls vocal production is poorly understood. Here, we investigate the dynamics of territorial vocal duels and song-matching in common nightingales ( Luscinia megarhynchos ). Using a combination of field observations, playback experiments and accelerometry, we find that wild nightingales readily modified the acoustic features of their song, matched the rival’s song and engaged more vigorously against vocal opponents with a shared song repertoire. Furthermore, we demonstrate that neurons in the sensorimotor nucleus HVC are tuned to specific song stimuli, potentially enabling context-specific integration of auditory information to facilitate matched song production. These findings highlight the crucial role of song recognition in allowing nightingales to adjust their vocalizations in response to specific social situations, demonstrating the complexity and adaptability of their communication system. Moreover, this study provides a new framework and model system for investigating online sensorimotor processing during dynamic vocal interactions.

Many animals, including humans, produce multimodal displays by combining acoustic with visual or vibratory signals [1–4]. However, the neural circuits that coordinate the production of multiple signals in a context-dependent manner are unknown. Multimodal behaviors could be produced by parallel circuits that independently integrate the external cues that trigger each signal. We find that multimodal signals in Drosophila are driven by a single circuit that integrates external sensory cues with internal motivational state and circuit dynamics. Drosophila males produce air-borne song and substrate-borne vibration during courtship and previous studies have identified neurons that drive courtship and singing, but the contexts and circuits that drive vibrations and coordinate multimodal signaling were not known [5–11]. We show that males produce song and vibration in distinct, largely non-overlapping contexts and that brain neurons that drive song also drive vibrations with cell-type specific dynamics and via separate pre-motor pathways. This circuit also coordinates multimodal signaling with ongoing behavior, namely locomotion, to drive vibrations only when the male’s vibrations can reach the female. A shared circuit facilitates the control of signal dynamics by external cues and motivational state through shared mechanisms like recurrence and mutual inhibition. A proof-of-concept circuit model shows that these motifs are sufficient to explain the behavioral dynamics. Our work shows how simple motifs can be combined in a single neural circuit to select and coordinate multiple behaviors.