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Petrucco, L.

Publications and source records attributed to Petrucco, L..

8 recordsLinked to original sources

Anatomical and functional organization of the interpeduncular nucleus in larval zebrafish

The habenulo-interpeduncular pathway is a highly conserved neural circuit across vertebrates, but the anatomical and functional architecture of the interpeduncular nucleus (IPN) remains poorly understood. Here, we use a combination of immunohistochemistry, volumetric electron microscopy (EM), and two-photon imaging to provide the first detailed characterization of the internal organization of the IPN in larval zebrafish. We show that the IPN receives extensive projections from the tegmentum, and reveal a strict segregation between the dorsal (dIPN) and ventral (vIPN) subcircuits, with minimal cross-communication. In the dIPN, we characterise in detail the inputs and outputs of r1{pi} neurons, which have been recently identified as representing the animals heading direction. In the vIPN, we identify six distinct glomerular structures, each exhibiting specific patterns of reciprocal connections and projection pathways. Finally, we demonstrate that the connectivity and spontaneous activity patterns of habenular axons are shaped by the local anatomical features of the IPN, suggesting a role for the local interneurons in modulating presynaptic dynamics. Together, these results enhance our understanding of the internal organization of the IPN, and provide a framework for future investigations into both its physiology and its involvement in behavior.

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The representation of visual motion and landmark position aligns with heading direction in the zebrafish interpeduncular nucleus

Sensory information is fundamental for navigation. Visual motion is used by animals to estimate their traveling distance and direction, and visual landmarks allow animals to tether their location and orientation to their environment. How such signals are integrated in the vertebrate brain is poorly understood. Here we investigate the representation of directional whole field visual motion and landmark position in a circuit in the larval zebrafish consisting of the habenula, interpeduncular nucleus (IPN) and anterior hindbrain (aHB). This circuit has been recently implicated in the representation of heading direction. Using calcium imaging we show that these stimuli are represented in the habenula, IPN and aHB. We further show that their representation in the IPN of both these stimuli is topographically arranged in a way that aligns itself with the representation of the heading signal in this region. We use neuronal ablations to show that the landmark responses, but not the whole field motion responses, require intact habenula input to the IPN. Overall our findings suggest the IPN as a site for integration of the heading signal from the aHB with visual information, shedding light on how different types of navigational signals are processed in the vertebrate brain.

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A mixed mechano-olfactory code for sniff-invariant odor representations

Sampling behaviors have sensory consequences that can hinder perceptual stability. In olfaction, sniffing affects early odor encoding, mimicking a sudden change in odor concentration. Here, we examined how the inhalation speed impacts the representation of odor concentration in the main olfactory cortex. Neurons combine the odor input with a global top-down signal preceding the sniff and a mechanosensory feedback generated by the air passage through the nose during an inhalation. Still, the population representation of concentration is remarkably sniff-invariant. This is because the mechanosensory and olfactory responses are uncorrelated within and across neurons. Thus, a faster odor inhalation and a concentration increase change the cortical activity pattern in distinct ways. This encoding strategy affords tolerance to potential concentration fluctuations caused by varying inhalation speeds. Since mechanosensory reafferences are widespread across sensory systems, the coding scheme described here may be a canonical strategy to mitigate the sensory ambiguities caused by movements.

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Comparing the representation of a simple visual stimulus across the cerebellar network

The cerebellum is a highly conserved structure of the vertebrate central nervous system that plays a role in the timing and calibration of motor sequences. Its function is supported by the convergence of fibers from granule cells (GCs) and inferior olive neurons (IONs) onto Purkinje cells (PCs). Theories of cerebellar function postulate that IONs convey error signals to PCs that, paired with the contextual information provided by GCs, can be used as a teaching signal to guide motor learning. Here, we use the larval zebrafish to investigate (i) how sensory representations of the same stimulus vary across GCs and IONs and (ii) how PC activity reflects these two different input streams. We use population calcium imaging to measure the cell responses to flashes of diverse luminance and duration to show that IONs and GCs encode different stimulus properties. First, most GCs show tonic and graded responses, as opposed to IONs, whose activity peaks only at on and off luminance transitions, in agreement with the notion that GCs and IONs encode context and error information, respectively. Secondly, we show that GC activity is patterned over time: some neurons had sustained responses for the entire duration of the stimulus, while in others activity was ramping up with slow time constants. This suggests that, by performing temporal integration, GCs could provide a basis that PCs may use to decode time. Finally, we show how PC activity can be largely reconstructed by a linear combination of granule cells and inferior olive neurons. Together, our observations give support to the notion of an error signal coming from IONs, and provide the first experimental evidence for a temporal patterning of GC activity over many seconds.

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Neural dynamics and architecture of the heading direction circuit in a vertebrate brain

Animals can use different strategies to navigate. They may guide their movements by relying on external cues in their environment or, alternatively, by using an internal cognitive map of the space around them and their position within it. An essential part of this representation are heading cells, neurons whose activity depends on the heading direction of the animal. Although those cells have been found in vertebrates, the full network has never been observed and there is very little mechanistic understanding of how these cells acquire their response properties. In this study, we use volumetric functional imaging in larval zebrafish to observe, for the first time in a vertebrate, a full network that encodes allocentric heading direction. This network of approximately one hundred inhibitory neurons is arranged in an anatomical circle in the anterior hindbrain. Its activity is driven purely by the integration of internally generated signals, indicating that a simple vertebrate brain can encode maps of how an animal moves within its surroundings. Single cell reconstructions of electron micrographs allow us to uncover how the connectivity pattern of neurons within the network supports the implementation of a ring attractor network. The neurons we identify share features with neurons in the dorsal tegmentum nucleus of rodents and the fly central complex, showing that similar connectivity and mechanistic principles underlie the generation of cognitive maps of heading direction across the animal kingdom.

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Oligodendrocyte Precursor Cells Sculpt the Visual System by Regulating Axonal Remodeling

Many oligodendrocyte precursor cells (OPCs) do not differentiate to form myelin, suggesting additional roles of this cell population. The zebrafish optic tectum contains OPCs in regions devoid of myelin. Elimination of these OPCs impaired precise control of retinal ganglion cell axon arbor size during formation and maturation of retinotectal connectivity, and in consequence impaired visual acuity. Therefore, OPCs fine-tune neural circuit structure and function independently of their canonical role to make myelin.

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The cerebellum recalibrates a feedback controller involved in motor control

Animals must adapt their behavior to survive in a changing environment. Behavioral adaptations can be evoked by two mechanisms: feedback control and internal-model-based control. Feedback controllers can maintain the sensory state of the animal at a desired level under different environmental conditions. In turn, internal models learn the relationship between behavior and resulting sensory consequences in order to modify the behavior when this relationship changes. Here, we present multiple perturbations in visual feedback to larval zebrafish performing the optomotor response and show that they react to these perturbations through a feedback control mechanism. In contrast, if a perturbation is long-lasting, fish adapt their behavior by updating a cerebellum-dependent internal model. We use modelling and functional imaging to show that neuronal requirements for these mechanisms are met in the larval zebrafish brain. Our results illustrate the role of the cerebellum in encoding internal models and how these can calibrate neuronal circuits involved in reactive behaviors depending on the interactions between animal and environment. HighlightsO_LIBehavioral reactions to unexpected changes in visual feedback are implemented by a feedback control mechanism C_LIO_LIA long-lasting change in visual feedback updates the state of the neuronal controller C_LIO_LIThe cerebellar internal model mediates this recalibration C_LI

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Stytra: an open-source, integrated system for stimulation, tracking and closed-loop behavioral experiments

We present Stytra, a flexible, open-source software package, written in Python, that we designed to cover all the general requirements involved in larval zebrafish behavioral experiments. It allows timed stimulus presentation, interfacing with external devices and simultaneous real-time tracking of position, tail and eye motion in both freely-swimming and head-restrained preparations. It logs in standardized formats all recorded quantities, metadata, and code version to allow full provenance tracking, from data acquisition through analysis to publication. The package is modular and expandable for different experimental protocols and setups. Current releases can be found at https://github.com/portugueslab/stytra. We also provide complete documentation with examples for extending the package to new stimuli and hardware, as well as a schema and parts list for behavioral setups. We showcase Stytra by reproducing two previously behavioral protocols, one with head-restrained and the other with freely-swimming larvae, as well as an experiment in which the software is used in the context of a calcium imaging experiment, where it can trigger and communicate with other acquisition devices. Our aims are to help laboratories with little or no experience in the field to start implementing behavioral experiments and to provide a platform for sharing stimulus protocols to enable easy reproduction of experiments and straightforward validation. In addition, Stytra can easily serve as a base platform to design behavioral experiments in other model organisms.

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