Person: Robson, Drew
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Robson
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Drew
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Robson, Drew
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Publication Gaze-Stabilizing Central Vestibular Neurons Project Asymmetrically to Extraocular Motoneuron Pools(Society for Neuroscience, 2017) Schoppik, David; Bianco, Isaac H.; Prober, David A.; Douglass, Adam D.; Robson, Drew; Li, Jennifer M.B.; Greenwood, Joel S.F.; Soucy, Edward; Engert, Florian; Schier, AlexanderWithin reflex circuits, specific anatomical projections allow central neurons to relay sensations to effectors that generate movements. A major challenge is to relate anatomical features of central neural populations, such as asymmetric connectivity, to the computations the populations perform. To address this problem, we mapped the anatomy, modeled the function, and discovered a new behavioral role for a genetically defined population of central vestibular neurons in rhombomeres 5–7 of larval zebrafish. First, we found that neurons within this central population project preferentially to motoneurons that move the eyes downward. Concordantly, when the entire population of asymmetrically projecting neurons was stimulated collectively, only downward eye rotations were observed, demonstrating a functional correlate of the anatomical bias. When these neurons are ablated, fish failed to rotate their eyes following either nose-up or nose-down body tilts. This asymmetrically projecting central population thus participates in both upward and downward gaze stabilization. In addition to projecting to motoneurons, central vestibular neurons also receive direct sensory input from peripheral afferents. To infer whether asymmetric projections can facilitate sensory encoding or motor output, we modeled differentially projecting sets of central vestibular neurons. Whereas motor command strength was independent of projection allocation, asymmetric projections enabled more accurate representation of nose-up stimuli. The model shows how asymmetric connectivity could enhance the representation of imbalance during nose-up postures while preserving gaze stabilization performance. Finally, we found that central vestibular neurons were necessary for a vital behavior requiring maintenance of a nose-up posture: swim bladder inflation. These observations suggest that asymmetric connectivity in the vestibular system facilitates representation of ethologically relevant stimuli without compromising reflexive behavior. SIGNIFICANCE STATEMENT Interneuron populations use specific anatomical projections to transform sensations into reflexive actions. Here we examined how the anatomical composition of a genetically defined population of balance interneurons in the larval zebrafish relates to the computations it performs. First, we found that the population of interneurons that stabilize gaze preferentially project to motoneurons that move the eyes downward. Next, we discovered through modeling that such projection patterns can enhance the encoding of nose-up sensations without compromising gaze stabilization. Finally, we found that loss of these interneurons impairs a vital behavior, swim bladder inflation, that relies on maintaining a nose-up posture. These observations suggest that anatomical specialization permits neural circuits to represent relevant features of the environment without compromising behavior.Publication Thermal navigation in larval zebrafish(2013-10-08) Robson, Drew; Schier, Alexander F; Engert, Florian; Sanes, Joshua; Samuel, Aravinthan; Ölveczky, BenceNavigation in complex environments requires selection of appropriate actions as a function of local cues. To gain a quantitative and mechanistic understanding of zebrafish thermal navigation, we have developed a novel assay that requires animals to rely exclusively on thermosensory information in the absence of other cues such as vision or mechanosensation. We show that zebrafish use both absolute and relative temperature information to restrict their locomotor trajectories to a preferred temperature range. We identify components of movement that are modulated solely by absolute temperature, as well as components that are modulated by both absolute and relative temperature. Specifically, we find that dwell time between movements and displacement per movement depend solely on absolute temperature, whereas turn magnitude and turn direction bias are modulated by absolute and relative temperature. To evaluate whether these sensorimotor relationships could explain thermal restriction in our navigation assay, we performed Monte Carlo simulations of locomotor trajectories based on all or subsets of these relationships. We find that thermosensory modulation of turn magnitude and turn direction bias constitute the core navigation strategy in larval zebrafish, while modulation of dwell time accelerates the execution of this strategy at noxious temperatures. Modulation of turn direction bias represents a novel strategy not found in invertebrate models, whereby animals correct unfavorable headings by preferentially turning in a preferred turn direction until they obtain a favorable heading. Modulating turn direction bias in response to recent sensory experience is an effective strategy for selecting favorable headings in organisms that do not have a dedicated sampling phase before each reorientation event.Publication The Tangential Nucleus Controls a Gravito-inertial Vestibulo-ocular Reflex(Elsevier, 2012) Bianco, Isaac; Ma, Leung-Hang; Schoppik, David; Robson, Drew; Orger, Michael B.; Beck, James C.; Li, Jennifer; Schier, Alexander; Engert, Florian; Baker, RobertWhilst adult vertebrates sense changes in head position using two classes of accelerometer, at larval stages zebrafish lack functional semicircular canals and rely exclusively on their otolithic organs to transduce vestibular information. Despite this limitation, they perform an effective vestibulo-ocular reflex (VOR) that serves to stabilize gaze in response to pitch and roll tilts. Using single-cell electroporations and targeted laser-ablations, we identified a specific class of central vestibular neurons, located in the tangential nucleus, which are essential for the utricle-dependent VOR. Tangential nucleus neurons project contralaterally to extraocular motoneurons, and in addition, to multiple sites within the reticulospinal complex. We propose that tangential neurons function as a broadband inertial accelerometer, processing utricular acceleration signals to control the activity of extraocular and postural neurons, thus completing a fundamental three-neuron circuit responsible for gaze stabilization.Publication Internal State Dynamics Shape Brainwide Activity and Foraging Behaviour(Springer Science and Business Media LLC, 2019-12-18) Marques, Joao; Li, Meng; Schaak, Diane; Robson, Drew; Li, Jennifer M.The brain has persistent internal states that can modulate every aspect of an animal’s mental experience(1–4). In complex tasks such as foraging, internal state is dynamic(5–8). C. elegans alternate between local search and global dispersal5. Rodents and primates exhibit trade-offs between exploitation and exploration(6,7). However, fundamental questions remain about how persistent states are maintained in the brain, which upstream networks drive state transitions, and how state-encoding neurons exert neuromodulatory effects on sensory perception and decision making to govern appropriate behavior. Using tracking microscopy in larval zebrafish9, we can monitor whole brain neuronal activity at cellular resolution in a freely moving animal across spontaneous internal state transitions. We show that larval zebrafish alternate between two persistent behavioral states during foraging for live prey (paramecia). In the exploitation state, the animal inhibits locomotion and promotes hunting, generating small localized trajectories. In the exploration state, the animal promotes locomotion and suppresses hunting, generating long ranging trajectories that enhance spatial dispersion. We uncover a dorsal raphe subpopulation with persistent activity that robustly encodes the exploitation state. The exploitation state-encoding neurons, together with a multimodal trigger network that is associated with state transitions, form a stochastically activated nonlinear dynamical system. The activity of this oscillatory network correlates with a global re-tuning of sensorimotor transformations during foraging that leads to dramatic changes in both the motivation to hunt for prey and the accuracy of motor sequences during hunting. This work reveals an important hidden variable that shapes the temporal structure of motivation and decision making.