Genetic Single-Cell Mosaic Analysis Implicates ephrinB2 Reverse Signaling in Projections from the Posterior Tectum to the Hindbrain in Zebrafish

Satō, Tomomi; Hamaoka, Takanori; Aizawa, Hidenori; Hosoya, Toshihiko; Okamoto, Hitoshi

doi:10.1523/jneurosci.0883-07.2007

Cited by 96 publications

(90 citation statements)

References 45 publications

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“…More obscure, however, is the upstream circuitry that leads to the selective activation of these descending control neurons. Recently developed optical techniques, which are capable of revealing activity and connectivity in large numbers of neurons [41][42][43] , can now be focused on determining the inputs to neurons with known response selectivities and identified roles in behavior. Together, this opens up the possibility of studying complete circuits underlying complex behaviors in a vertebrate with a small, transparent brain.…”

Section: Discussionmentioning

confidence: 99%

Control of visually guided behavior by distinct populations of spinal projection neurons

et al. 2008

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A basic question in the field of motor control is how different actions are represented by activity in spinal projection neurons. We used a new behavioral assay to identify visual stimuli that specifically drive basic motor patterns in zebrafish. These stimuli evoked consistent patterns of neural activity in the neurons projecting to the spinal cord, which we could map throughout the entire population using in vivo two-photon calcium imaging. We found that stimuli that drive distinct behaviors activated distinct subsets of projection neurons, consisting, in some cases, of just a few cells. This stands in contrast to the distributed activation seen for more complex behaviors. Furthermore, targeted cell by cell ablations of the neurons associated with evoked turns abolished the corresponding behavioral response. This description of the functional organization of the zebrafish motor system provides a framework for identifying the complete circuit underlying a vertebrate behavior.In a behaving animal, the brain communicates its intentions to muscles via the pattern of activity in descending projection neurons 1 . In vertebrates, these cells respond to the detection and processing of sensory stimuli and transmit their motor command to the local networks of the spinal cord, which in turn initiate and coordinate muscle contraction 2 . A fundamental question in neuroscience is how the commands that initiate behaviors are encoded in the activation of these projection neurons 3-5 .The spinal projection system of fish provides an excellent model for studying this code 6 . A diverse range of swimming behaviors can be seen in 6-d-old zebrafish 7-9 that are mediated by a descending projection to the spinal cord consisting of fewer than 300 neurons 10,11 . These neurons are easily labeled with fluorescent indicators 12 , optically accessible with modern imaging techniques and arranged in a stereotyped pattern such that the same cells or groups of cells can easily be identified from one fish to the next 13 . These neurons are morphologically diverse, with distinct dendritic fields and axonal projection patterns 13,14 , suggesting that they serve different behavioral functions. Nevertheless, determining how differing patterns of activity in these spinal projection neurons produce different motor outputs has proved to be difficult. 23,24 , the actual command is encoded in distributed activity throughout the population of control neurons 2 .The swimming behaviors of zebrafish, including the complex sequence of turns and swims that make up the escape response, can be broken down into basic kinematic elements 8 . It is possible that the motor commands for these basic behaviors originate from distinct populations of neurons, which when combined would appear as a `distributed command'. We found that whole-field visual motion, with the direction dynamically locked to the fish's body axis, is able to selectively evoke some of these basic swim patterns. Calcium imaging of stimulus-evoked responses in the complete population of n...

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Section: Discussionmentioning

confidence: 99%

Control of visually guided behavior by distinct populations of spinal projection neurons

et al. 2008

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“…Neurons in the tectum project to reticulospinal regions in the larval zebrafish (Sato et al, 2007). Turn intensity control via reticulospinal neurons in zebrafish larvae has been studied in the context of fast evasive maneuvers, like those generated during escapes.…”

Section: Circuit Mechanisms Governing Approachmentioning

confidence: 99%

Visually guided gradation of prey capture movements in larval zebrafish

Patterson

Abraham

MacIver

et al. 2013

Journal of Experimental Biology

107

155

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SUMMARYA mechanistic understanding of goal-directed behavior in vertebrates is hindered by the relative inaccessibility and size of their nervous systems. Here, we have studied the kinematics of prey capture behavior in a highly accessible vertebrate model organism, the transparent larval zebrafish (Danio rerio), to assess whether they use visual cues to systematically adjust their movements. We found that zebrafish larvae scale the speed and magnitude of turning movements according to the azimuth of one of their standard prey, paramecia. They also bias the direction of subsequent swimming movements based on prey azimuth and select forward or backward movements based on the prey's direction of travel. Once within striking distance, larvae generate either ram or suction capture behaviors depending on their distance from the prey. From our experimental estimations of ocular receptive fields, we ascertained that the ultimate decision to consume prey is likely a function of the progressive vergence of the eyes that places the target in a proximal binocular 'capture zone'. By repeating these experiments in the dark, we demonstrate that paramecia are only consumed if they contact the anterior extremities of larvae, which triggers ocular vergence and tail movements similar to close proximity captures in lit conditions. These observations confirm the importance of vision in the graded movements we observe leading up to capture of more distant prey in the light, and implicate somatosensation in captures in the absence of light. We discuss the implications of these findings for future work on the neural control of visually guided behavior in zebrafish. Supplementary material available online at

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“…Their axonal projections excite spinal central pattern generators (CPGs) that drive coordinated rhythmic swimming activity (Deliagina et al, 2002). Interestingly, both the escape and swim circuits receive visual and postural sensory information (Sato et al, 2007;Kohashi and Oda, 2008;Mu et al, 2012) and are regulated by neuromodulatory inputs (Pereda et al, 1992;McLean and Fetcho, 2004). This suggests that the circuits and the behaviors they produce may be susceptible to plastic changes influenced by social experience.…”

Section: Introductionmentioning

confidence: 99%

Social Status–Dependent Shift in Neural Circuit Activation Affects Decision Making

Miller¹,

Clements²,

Ahn

et al. 2017

J. Neurosci.

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In a social group, animals make behavioral decisions that fit their social ranks. These behavioral choices are dependent on the various social cues experienced during social interactions. In vertebrates, little is known of how social status affects the underlying neural mechanisms regulating decision-making circuits that drive competing behaviors. Here, we demonstrate that social status in zebrafish (Danio rerio) influences behavioral decisions by shifting the balance in neural circuit activation between two competing networks (escape and swim). We show that socially dominant animals enhance activation of the swim circuit. Conversely, social subordinates display a decreased activation of the swim circuit, but an enhanced activation of the escape circuit. In an effort to understand how social status mediates these effects, we constructed a neurocomputational model of the escape and swim circuits. The model replicates our findings and suggests that social status-related shift in circuit dynamics could be mediated by changes in the relative excitability of the escape and swim networks. Together, our results reveal that changes in the excitabilities of the Mauthner command neuron for escape and the inhibitory interneurons that regulate swimming provide a cellular mechanism for the nervous system to adapt to changes in social conditions by permitting the animal to select a socially appropriate behavioral response.

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Genetic Single-Cell Mosaic Analysis Implicates ephrinB2 Reverse Signaling in Projections from the Posterior Tectum to the Hindbrain in Zebrafish

Cited by 96 publications

References 45 publications

Control of visually guided behavior by distinct populations of spinal projection neurons

Control of visually guided behavior by distinct populations of spinal projection neurons

Visually guided gradation of prey capture movements in larval zebrafish

Social Status–Dependent Shift in Neural Circuit Activation Affects Decision Making

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