Classification of Object Size in Retinotectal Microcircuits

Preuss, Stephanie J.; Trivedi, Chintan A.; Berg, Colette vom; Ryu, Soojin; Bollmann, Johann H.

doi:10.1016/j.cub.2014.09.012

Cited by 103 publications

(153 citation statements)

References 47 publications

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“…In order to dissect the role of individual neural components of tectal circuitry in generating the population activity encoding critical angle, we analyzed activity patterns in two distinct neural cell types: retinal ganglion cells (RGCs) that send axons into the four input layers of the OT (SO, SFGS, SGC, SAC, (Nikolaou et al, 2012)), and superficial inhibitory interneurons (SINs), which have been shown to play a significant role in filtering out large (Del Bene et al, 2010) as well as small (Preuss et al, 2014) moving visual stimuli. In order to measure activity in RGC terminals, we generated a transgenic fish line (UAS:SyGCaMP6s) in which GCaMP6s (Chen et al, 2013) is linked to synaptophysin and expression in RGCs is driven by an Isl2b:Gal4 line (Figure 4A (Nikolaou et al, 2012)).…”

Section: Resultsmentioning

confidence: 99%

Neural Circuits Underlying Visually Evoked Escapes in Larval Zebrafish

Dunn

Gebhardt

Naumann

et al. 2016

Neuron

290

358

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SUMMARY Escape behaviors deliver organisms away from imminent catastrophe. Here, we characterize behavioral responses of freely swimming larval zebrafish to looming visual stimuli simulating predators. We report that the visual system alone can recruit lateralized, rapid escape motor programs, similar to those elicited by mechanosensory modalities. Two-photon calcium imaging of retino-recipient midbrain regions isolated the optic tectum as an important center processing looming stimuli, with ensemble activity encoding the critical image size determining escape latency. Furthermore, we describe activity in retinal ganglion cell terminals and superficial inhibitory interneurons in the tectum during looming and propose a model for how temporal dynamics in tectal periventricular neurons might arise from computations between these two fundamental constituents. Finally, laser ablations of hindbrain circuitry confirmed that visual and mechanosensory modalities share the same premotor output network. Together, we establish a circuit for the processing of aversive stimuli in the context of an innate visual behavior.

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Section: Resultsmentioning

confidence: 99%

Neural Circuits Underlying Visually Evoked Escapes in Larval Zebrafish

Dunn

Gebhardt

Naumann

et al. 2016

Neuron

290

358

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“…When this nutrient need was met, nutrient intake dropped, and larvae were satiated. This behavior occurred on a 2-h timescale and likely modulated the visual-motor programs required for hunting behavior (4,26,33). Upon meal ingestion, food is digested within the gastrointestinal tract.…”

Section: Discussionmentioning

confidence: 99%

A high-throughput assay for quantifying appetite and digestive dynamics

Jordi

Guggiana-Nilo

Soucy

et al. 2015

American Journal of Physiology-Regulatory, Integrative and Comp

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Jordi J, Guggiana-Nilo D, Soucy E, Song EY, Wee CL, Engert F. A high-throughput assay for quantifying appetite and digestive dynamics. Am J Physiol Regul Integr Comp Physiol 309: R345-R357, 2015. First published June 24, 2015 doi:10.1152/ajpregu.00225.2015.-Food intake and digestion are vital functions, and their dysregulation is fundamental for many human diseases. Current methods do not support their dynamic quantification on large scales in unrestrained vertebrates. Here, we combine an infrared macroscope with fluorescently labeled food to quantify feeding behavior and intestinal nutrient metabolism with high temporal resolution, sensitivity, and throughput in naturally behaving zebrafish larvae. Using this method and rate-based modeling, we demonstrate that zebrafish larvae match nutrient intake to their bodily demand and that larvae adjust their digestion rate, according to the ingested meal size. Such adaptive feedback mechanisms make this model system amenable to identify potential chemical modulators. As proof of concept, we demonstrate that nicotine, L-lysine, ghrelin, and insulin have analogous impact on food intake as in mammals. Consequently, the method presented here will promote large-scale translational research of food intake and digestive function in a naturally behaving vertebrate.appetite; hunger; satiation; satiety; DiR' dye FOOD INTAKE AND DIGESTION are key physiological processes that provide nutrients to drive all bodily functions. Nutrient intake is matched to nutritional needs by the brain-a process termed nutrient homeostasis-using an intertwined organism-wide array of extrinsic and intrinsic cues coding food availability and demand (2, 42). Dysfunction of feeding and digestive behavior is at the root of global health problems, such as obesity, malnutrition, and Type 2 diabetes, among many others, and, therefore, a deeper understanding of feeding and digestive behavior is of high importance (25).Drugs or genetic manipulations that alter food intake or digestion are highly desirable remedies for food-related disorders. To screen for genes or small molecules with clinically desirable impact, the technology of choice needs to support the analyses of hundreds to thousands of individual animals. Until now, large-scale studies of feeding behavior have solely been feasible in small invertebrates such as Drosophila, but were constrained to 20 -50 conditions in vertebrates, thereby making large-scale screens elusive (12,17,35). Technically, even more demanding than measuring food intake is the quantification of nutrient digestion, as there is no direct optical access to the gastrointestinal tract in most species. More specialized technologies, such as bioluminescence, MRI, or computed tomography, have been valuable to generate insights into in vivo dynamics of digestive function (10,18,19,31). However, all of these methods require immobilization of the experimental subject to reduce motion artifacts, thereby making concurrent behavioral observations impossible. Consequently, quantifying the dy...

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“…Although it has been shown that tectal cells have preferences for particular stimuli features (Bianco & Engert, 2015;Hunter et al, 2013;Preuss et al, 2014), the cells responding as part of an assembly can vary across trials. To determine whether the cells in our trials were responding consistently, the matching index (MI) was calculated for each assembly across the five trials in each animal (Romano et al, 2015).…”

Section: Assemblies Are Highly Variable Trial To Trial But Contain Rmentioning

confidence: 99%

“…While the different roles of two classes of core cells described above remain unknown, they may represent activation of different populations of inhibitory interneurons versus excitatory, efferent cells. Inhibitory neurons have been shown to be critical in the zebrafish tectum to the filtering of large visual information , Preuss et al, 2014 and are also likely to influence direction selectivity (Grama & Engert, 2012). Likely to be an important direction for future research will be determining the role of these cells in deciding which networks of cells become activated in response to particular stimuli.…”

Section: Assembly Coresmentioning

confidence: 99%

“…While current literature has focused primarily on the methodology of the imaging, the results presented in Chapter 4 of this thesis utilise this technique to analyse the functional activity of a given neural circuit, namely that responsible for sensory perception in the zebrafish tectum. A large number of studies have examined the tectum of larval zebrafish in order to understand visual processing (Bianco & Engert, 2015;Del Bene et al, 2010;Hunter et al, 2013;Nikolaou et al, 2012;Preuss et al, 2014;Romano et al, 2015;Temizer et al, 2015), but this thesis aimed to extend this knowledge and study the response profiles of cells in the tectum to non-visual sensory modalities, a function known to be important in the homologous mammalian region. Until now this function of the tectum has been unexplored in larval zebrafish, and as such the results here provide a novel contribution to the field.…”

Section: Overviewmentioning

confidence: 99%

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Functional investigation of neural circuits in larval zebrafish

Thompson¹

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A fundamental goal of modern neuroscience is to understand the principles by which neural circuits within the brain lead to cognition and behaviour. Technological advances in the fields of microscopy and optogenetics have very recently allowed for the activity of all cells within a functional circuit to be observed and recorded, meaning that this goal is now within reach. Due to the physical and optical properties of neural tissue, these technologies remain most useful for the analysis of circuits that span very small volumes, meaning that small animal model organisms, with brains less than approximately 1 mm across, are most amenable to these types of analyses. The larval zebrafish model has emerged as an optimal balance between small size and the high complexity of a vertebrate brain. This thesis describes the development and application of several of these technological advances to examine neural circuits underlying perception and behaviour in the larval zebrafish.Due to the relative recency of zebrafish as a model for functional neuroscience, the genetic and experimental tools required for in depth circuit analysis have not been widely available. Thirteen transgenic zebrafish lines have been developed during this thesis for expressing optogenetic proteins throughout the brain, such as GCaMP5G for imaging neuronal calcium dynamics, and ChR2(ET/TC) and eNpHR3.0 for activating and silencing neuronal activity, respectively. These biological tools were developed in combination with optical techniques for probing neural circuits. This thesis describes the design and construction of a custom selective plane illumination microscope for the rapid imaging of neuronal activity across large areas of the zebrafish brain. The use of a spatial light modulator is also described for the targeted stimulation of ChR2(ET/TC) in the cerebellum of larval zebrafish. This experiment provided preliminary data for the functional investigation of connections between cerebellar cells and the optic tectum, as well as confirming the validity of this technique for analysis of other neuronal circuits in vivo.Since learning is one of the most interesting yet ill-defined processes controlled by the brain, this thesis aimed to use the tools developed above to examine the changes across neuronal circuit activity responsible for learning in larval zebrafish, specifically those in the cerebellum responsible for motor learning. A classical P ag e 2 conditioning assay was administered to 7-day-old zebrafish by pairing a non-startling tone with an aversive tail shock stimulus. This paradigm has been extensively used in other model organisms, however failed to produce a significant learning behaviour in the experiments performed for this thesis. More recent evidence suggests that zebrafish only begin to show learning from approximately one month of age.However, the data presented here indicate that zebrafish up to six weeks of age were still unable to undergo classical conditioning to pairings of auditory and electric stimuli. A number of is...

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Classification of Object Size in Retinotectal Microcircuits

Abstract: Ethologically relevant size classes are preferentially processed in different layers of the tectal neuropil. The tectum categorizes visual targets on the basis of retinally computed size information, suggesting a critical role in visually guided response selection.

Cited by 103 publications

References 47 publications

Neural Circuits Underlying Visually Evoked Escapes in Larval Zebrafish

Neural Circuits Underlying Visually Evoked Escapes in Larval Zebrafish

A high-throughput assay for quantifying appetite and digestive dynamics

Functional investigation of neural circuits in larval zebrafish

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