Behavioral Neuroscience seminars

A globally invasive form of the mosquito Aedes aegypti has evolved to specialize in biting humans, making it an efficient vector of dengue, yellow fever, Zika, and chikungunya. Host-seeking females identify humans primarily by smell, strongly preferring human odour over the odor of non-human animals. Exactly how they discriminate, however, is unclear. Human and animal odors are complex blends that share most of the same chemical components, presenting an interesting challenge in sensory coding. I will talk about recent work from the lab showing that (1) human and animal blends can be distinguished by the relative concentration of a diverse array of compounds and that (2) these complex chemical differences translate into a neural code for human odor that involves as few as two to three olfactory glomeruli in the mosquito brain. Our work demonstrates how organisms may evolve to discriminate complex odor stimuli of special biological relevance with a surprisingly simple combinatorial code and reveals novel targets for the design of next-generation mosquito control strategies.

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.

The neural mechanisms underlying decision-making are typically examined by statistical analysis of large numbers of trials from sequentially recorded single neurons. Averaging across sequential recordings, however, obscures important aspects of decision-making such as variations in confidence and 'changes of mind' (CoM) that occur at variable times on different trials. I will show that the covert decision variables (DV) can be tracked dynamically on single behavioral trials via simultaneous recording of large neural populations in prefrontal cortex. Vacillations of the neural DV, in turn, identify candidate CoM in monkeys, which closely match the known properties of human CoM. Thus simultaneous population recordings can provide insight into transient, internal cognitive states that are otherwise undetectable.

behaviour varies even among genetically identical animals raised in the same environment. However, little is known about the circuit or anatomical underpinnings of this individuality, though previous work implicates sensory periphery. Drosophila olfaction presents an ideal model to study the biological basis of behavioural individuality, because while the neural circuit underlying olfactory behaviour is well-described and highly stereotyped, persistent idiosyncrasy in behaviour, neural coding, and neural wiring have also been described. Projection neurons (PNs), which relay odor signals sensed by olfactory receptor neurons (ORNs) to deeper brain structures, exhibit variable calcium responses to identical odor stimuli across individuals, but how these idiosyncrasies relate to individual behavioural responses remains unknown. Here, using paired behaviour and two-photon imaging measurements, we show that idiosyncratic calcium dynamics in both ORNs and PNs predict individual preferences for an aversive monomolecular odorant versus air, suggesting that variation at the periphery of the olfactory system determines individual preference for an odor’s presence. In contrast, PN, but not ORN, calcium responses predict individual preferences in a two-odor choice assay. Furthermore, paired behaviour and immunohistochemistry measurements reveal that variation in ORN presynaptic density also predicts two-odor preference, suggesting this site is a locus of individuality where microscale circuit variation gives rise to idiosyncrasy in behaviour. Our results demonstrate how a neural circuit may vary functionally and structurally to produce variable behaviour among individuals.

The dominant view of perception right now is that information travels from the environment to the sensory system, then to the nervous systems which processes it to generate a percept and behaviour. Ongoing behaviour is thought to occur largely through simple iterations of this process. However, this linear view, where information flows only in one direction and the properties of the environment and the sensory system remain static and unaffected by behaviour, is slowly fading. Many of us are beginning to appreciate that perception is largely active, i.e. that information flows back and forth between the three systems modulating their respective properties. In other words, in the real world, the environment and sensorimotor loop is pretty much always closed. I study the loop; in particular I study how the reverse arm of the loop affects sound and vibration perception. I will present two examples of motor modulation of perception at two very different temporal and spatial scales. First, in crickets, I will present data on how high-speed molecular motor activity enhances hearing via the well-studied phenomenon of active amplification. Second, in spiders I will present data on how body posture, a slow macroscopic feature, which can barely be called ‘active’, can nonetheless modulate vibration perception. I hope these results will motivate a conversation about whether ‘active’ perception is an optional feature observed in some sensory systems, or something that is ultimately necessitated by both evolution and physics.

How does our brain rapidly determine if something is good or bad? How do we know our place within a social group? How do we know how to behave appropriately in dynamic environments with ever-changing conditions? The Tye Lab is interested in understanding how neural circuits important for driving positive and negative motivational valence (seeking pleasure or avoiding punishment) are anatomically, genetically and functionally arranged. We study the neural mechanisms that underlie a wide range of behaviours ranging from learned to innate, including social, feeding, reward-seeking and anxiety-related behaviours. We have also become interested in “social homeostasis” -- how our brains establish a preferred set-point for social contact, and how this maintains stability within a social group. How are these circuits interconnected with one another, and how are competing mechanisms orchestrated on a neural population level? We employ optogenetic, electrophysiological, electrochemical, pharmacological and imaging approaches to probe these circuits during behaviour.

Inhibitory microcircuits play an important role regulating cortical responses to sensory stimuli. Interneurons that inhibit dendritic or somatic integration are gatekeepers for neural activity, synaptic plasticity and the formation of sensory representations. We have been investigating the synaptic plasticity mechanisms underlying the formation of ensembles in olfactory and orbitofrontal cortex. We have been focusing on the roles of three inhibitory neuron classes in gating excitatory synaptic plasticity in olfactory cortex- somatostatin (SST-INs), parvalbumin (PV-INs), and vasoactive intestinal polypeptide (VIP-INs) interneurons. Further, we are investigating the rules for inhibitory plasticity and a potential role in stabilizing ensembles in associative cortices. I will present new findings to support distinct roles for different interneuron classes in the gating and stabilization of ensemble representations of olfactory responses.

How nervous systems control behaviour is the main question we seek to answer in neuroscience. Although visual systems have been a popular entry point into the brain, we don’t understand—in any deep sense—how visual perception guides navigation in flies (or any organism). I will present recent progress towards this goal from our lab. We are using anatomical insights from connectomics, genetic methods for labelling and manipulating identified cell types, neurophysiology, behaviour, and computational modeling to explain how the fly brain processes visual motion to regulate behaviour.

Many visual systems can process information in dynamically changing environments. In general, visual perception scales with changes in the visual stimulus, or contrast, irrespective of background illumination. This is achieved by adaptation. However, visual perception is challenged when adaptation is not fast enough to deal with sudden changes in overall illumination, for example when gaze follows a moving object from bright sunlight into a shaded area. We have recently shown that the visual system of the fly found a solution by propagating a corrective luminance-sensitive signal to higher processing stages. Using in vivo two-photon imaging and behavioural analyses we showed that distinct OFF-pathway inputs encode contrast and luminance. The luminance-sensitive pathway is particularly required when processing visual motion in contextual dim light, when pure contrast sensitivity underestimates the salience of a stimulus. Recent work in the lab has addressed the question how two visual pathways obtain such fundamentally different sensitivities, given common photoreceptor input. We are furthermore currently working out the network-based strategies by which luminance- and contrast-sensitive signals are combined to guide appropriate visual behaviour. Together, I will discuss the molecular, cellular, and circuit mechanisms that ensure contrast computation, and therefore robust vision, in fast changing visual scenes.

During conversations we rapidly switch between listening and speaking which often requires withholding or delaying our speech in order to hear others and avoid overlapping. This capacity for vocal turn-taking is exhibited by non-linguistic species as well, however the neural circuit mechanisms that enable us to regulate the precise timing of our vocalizations during interactions are unknown. We aim to identify the neural mechanisms underlying the coordination of vocal interactions. Therefore, we paired zebra finches with a vocal robot (1Hz call playback) and measured the bird’s call response times. We found that individual birds called with a stereotyped delay in respect to the robot call. Pharmacological inactivation of the premotor nucleus HVC revealed its necessity for the temporal coordination of calls. We further investigated the contributing neural activity within HVC by performing intracellular recordings from premotor neurons and inhibitory interneurons in calling zebra finches. We found that inhibition is preceding excitation before and during call onset. To test whether inhibition guides call timing we pharmacologically limited the impact of inhibition on premotor neurons. As a result zebra finches converged on a similar delay time i.e. birds called more rapidly after the vocal robot call suggesting that HVC inhibitory interneurons regulate the coordination of social contact calls. In addition, we aim to investigate the vocal turn-taking capabilities of the common nightingale. Male nightingales learn over 100 different song motifs which are being used in order to attract mates or defend territories. Previously, it has been shown that nightingales counter-sing with each other following a similar temporal structure to human vocal turn-taking. These animals are also able to spontaneously imitate a motif of another nightingale. The neural mechanisms underlying this behaviour are not yet understood. In my lab, we further probe the capabilities of these animals in order to access the dynamic range of their vocal turn taking flexibility.

The “Nature versus Nurture” debate on the origin of behaviour has long been dominated by a genome versus experience dichotomy. However, evidence that genetically identical individuals kept under identical conditions are behaviourally different is incontrovertible. Where might such individuality come from? Neither genes nor the environment directly encode behaviour. They encode or influence processes, notably the development of neuronal circuits, that in turn control behaviour. An understanding of how neuronal circuits develop and function at the individual organism level is therefore essential for understanding the origin of individuals. I will discuss our efforts to address this issue over the past decade using the Drosophila fruit fly as a model system.