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Donovan, J. C.

Publications and source records attributed to Donovan, J. C..

3 recordsLinked to original sources

Positional information drives distinct traits in transcriptomically identified neuronal types

Neuronal phenotypic traits such as morphology, connectivity, and function are dictated, to a large extent, by a specific combination of differentially expressed genes. Clusters of neurons in transcriptomic space correspond to distinct cell types and in some cases (e. g., C. elegans neurons1 and retinal ganglion cells2-4) have been shown to share morphology and function. The zebrafish optic tectum is composed of a spatial array of neurons that transforms visual inputs into motor outputs. While the visuotopic map is continuous, subregions of the tectum are functionally specialized5,6. To uncover the cell-type architecture of the tectum, we transcriptionally profiled its neurons, revealing more than 60 cell types that are organized in distinct anatomical layers. We then measured the visual responses of thousands of tectal neurons by two-photon calcium imaging and matched them with their transcriptional profile. Furthermore, we characterized the morphologies of transcriptionally identified neurons using specific transgenic lines. Surprisingly, we found that neurons that are transcriptionally similar can diverge functionally and morphologically. Incorporating the spatial coordinates of neurons within the tectal volume revealed functionally and morphologically defined anatomical subclusters within individual transcriptomic clusters. Our findings demonstrate that extrinsic, position-dependent factors expand the phenotypic repertoire of genetically similar neurons.

neuroscience↗

Deconstructing hunting behavior reveals a tightly coupled stimulus-response loop

Animals build behavioral sequences out of simple stereotyped actions. A comprehensive characterization of these actions and the rules underlying their temporal organization is necessary to understand sensorimotor transformations performed by the brain. Here, we use unsupervised methods to study behavioral sequences in zebrafish larvae. Generating a map of swim bouts, we reveal that fish modulate their tail movements along a continuum. We cluster bouts that share common kinematic features and contribute to similar behavioral sequences into seven modules. Behavioral sequences comprising a subset of modules bring prey into the anterior dorsal visual field of the larvae. Fish then release a capture maneuver comprising a stereotyped jaw movement and fine-tuned stereotyped tail movements to capture prey at various distances. We demonstrate that changes to chaining dynamics, but not module production, underlie prey capture deficits in two visually impaired mutants. Our analysis thus reveals the temporal organization of a vertebrate hunting behavior, with the implication that different neural architectures underlie prey pursuit and capture.

neuroscience↗

Neuronal circuitry for stimulus selection in the visual system

Visual objects naturally compete for the brains attention, and selecting just one of them for a behavioural response is often crucial for the animals survival1. The neural correlate of such stimulus prioritisation might take the form of a saliency map by which responses to one target are enhanced relative to distractors in other parts of the visual field2. Single-cell responses consistent with this type of computation have been observed in the tectum of primates, birds, turtles and lamprey2-7. However, the exact circuit implementation has remained unclear. Here we investigated the underlying neuronal mechanism presenting larval zebrafish with two simultaneous looming stimuli, each of which was able to trigger directed escapes on their own. Behaviour tracking revealed that the fish respond to these competing stimuli predominantly with a winner-take-all strategy. Using brain-wide functional recordings, we discovered neurons in the tectum whose responses to the target stimulus were non-linearly modulated by the saliency of the distractor. When the two stimuli were presented monocularly in different positions of the visual field, stimulus selection was already apparent in the activity of retinal ganglion cell axons, a likely consequence of antagonistic mechanisms operating outside the classical receptive field8,9. When the two stimuli were presented binocularly, i.e., on opposite sides of the fish, our analysis indicates that a loop involving excitatory and inhibitory neurons in the nucleus isthmi (NI) and the tectum weighed stimulus saliencies across hemispheres. Consistent with focal enhancement and global suppression, glutamatergic NI cells branch locally in the tectum, whereas GABAergic NI cells project broadly across both tectal hemispheres. Moreover, holographic optogenetic stimulation confirmed that glutamatergic NI neurons can modulate visual responses in the tectum. Together, our study shows, for the first time, context-dependent contributions of retinotectal and isthmotectal circuits to the computation of the visual saliency map, a prerequisite for stimulus-driven, bottom-up attention.

neuroscience↗