Activation of the hypothalamic feeding centre upon visual prey detection

The visual system plays a major role in food/prey recognition in diurnal animals, and food intake is regulated by the hypothalamus. However, whether and how visual information about prey is conveyed to the hypothalamic feeding centre is largely unknown. Here we perform real-time imaging of neuronal activity in freely behaving or constrained zebrafish larvae and demonstrate that prey or prey-like visual stimuli activate the hypothalamic feeding centre. Furthermore, we identify prey detector neurons in the pretectal area that project to the hypothalamic feeding centre. Ablation of the pretectum completely abolishes prey capture behaviour and neurotoxin expression in the hypothalamic area also reduces feeding. Taken together, these results suggest that the pretecto-hypothalamic pathway plays a crucial role in conveying visual information to the feeding centre. Thus, this pathway possibly converts visual food detection into feeding motivation in zebrafish.

[1]  R. Anadón,et al.  Gustatory and general visceral centers and their connections in the brain of adult zebrafish: a carbocyanine dye tract‐tracing study , 2017, The Journal of comparative neurology.

[2]  Jenna R. Sternberg,et al.  Optimization of a Neurotoxin to Investigate the Contribution of Excitatory Interneurons to Speed Modulation In Vivo , 2016, Current Biology.

[3]  Alessandro Filosa,et al.  Feeding State Modulates Behavioral Choice and Processing of Prey Stimuli in the Zebrafish Tectum , 2016, Neuron.

[4]  R. Wise,et al.  Lateral hypothalamic circuits for feeding and reward , 2016, Nature Neuroscience.

[5]  K. Kawakami,et al.  Calcium Imaging of Neuronal Activity in Free-Swimming Larval Zebrafish. , 2016, Methods in molecular biology.

[6]  K. Kawakami,et al.  Gal4 Driver Transgenic Zebrafish: Powerful Tools to Study Developmental Biology, Organogenesis, and Neuroscience. , 2016, Advances in genetics.

[7]  Herwig Baier,et al.  Sensorimotor Decision Making in the Zebrafish Tectum , 2015, Current Biology.

[8]  G. Sumbre,et al.  A microfluidic device to study neuronal and motor responses to acute chemical stimuli in zebrafish , 2015, Scientific Reports.

[9]  H. Baier,et al.  Figures and Figure Supplements , 2022 .

[10]  F. Engert,et al.  Visuomotor Transformations Underlying Hunting Behavior in Zebrafish , 2015, Current Biology.

[11]  Germán Sumbre,et al.  Spontaneous Neuronal Network Dynamics Reveal Circuit’s Functional Adaptations for Behavior , 2015, Neuron.

[12]  H. Abe,et al.  Connections of the commissural nucleus of Cajal in the goldfish, with special reference to the topographic organization of ascending visceral sensory pathways , 2015, The Journal of comparative neurology.

[13]  Karl Deisseroth,et al.  Visualizing Hypothalamic Network Dynamics for Appetitive and Consummatory Behaviors , 2015, Cell.

[14]  H. Baier,et al.  A dedicated visual pathway for prey detection in larval zebrafish , 2014, eLife.

[15]  Johann H. Bollmann,et al.  Classification of Object Size in Retinotectal Microcircuits , 2014, Current Biology.

[16]  Herwig Baier,et al.  The Retinal Projectome Reveals Brain-Area-Specific Visual Representations Generated by Ganglion Cell Diversity , 2014, Current Biology.

[17]  Malcolm A. MacIver,et al.  Visually guided gradation of prey capture movements in larval zebrafish , 2013, Journal of Experimental Biology.

[18]  Stefan R. Pulver,et al.  Ultra-sensitive fluorescent proteins for imaging neuronal activity , 2013, Nature.

[19]  Junichi Nakai,et al.  Real-Time Visualization of Neuronal Activity during Perception , 2013, Current Biology.

[20]  Florian Engert,et al.  Prey Capture Behavior Evoked by Simple Visual Stimuli in Larval Zebrafish , 2011, Front. Syst. Neurosci..

[21]  H. Berthoud,et al.  The lateral hypothalamus as integrator of metabolic and environmental needs: From electrical self-stimulation to opto-genetics , 2011, Physiology & Behavior.

[22]  Junichi Nakai,et al.  Genetic visualization with an improved GCaMP calcium indicator reveals spatiotemporal activation of the spinal motor neurons in zebrafish , 2011, Proceedings of the National Academy of Sciences.

[23]  Koichi Kawakami,et al.  Tol2-mediated transgenesis, gene trapping, enhancer trapping, and the Gal4-UAS system. , 2011, Methods in cell biology.

[24]  Ethan K. Scott,et al.  Filtering of Visual Information in the Tectum by an Identified Neural Circuit , 2010, Science.

[25]  Akihiro Urasaki,et al.  zTrap: zebrafish gene trap and enhancer trap database , 2010, BMC Developmental Biology.

[26]  N. Yamamoto,et al.  Ascending general visceral sensory pathways from the brainstem to the forebrain in a cichlid fish, Oreochromis (Tilapia) niloticus , 2010, The Journal of comparative neurology.

[27]  C. Rueden,et al.  Metadata matters: access to image data in the real world , 2010, The Journal of cell biology.

[28]  Akihiro Urasaki,et al.  Olfactory neural circuitry for attraction to amino acids revealed by transposon-mediated gene trap approach in zebrafish , 2009, Proceedings of the National Academy of Sciences.

[29]  Masahiko Hibi,et al.  Genetic dissection of neural circuits by Tol2 transposon-mediated Gal4 gene and enhancer trapping in zebrafish , 2008, Proceedings of the National Academy of Sciences.

[30]  Herwig Baier,et al.  Transactivation from Gal4-VP16 transgenic insertions for tissue-specific cell labeling and ablation in zebrafish. , 2007, Developmental biology.

[31]  Herwig Baier,et al.  Targeting neural circuitry in zebrafish using GAL4 enhancer trapping , 2007, Nature Methods.

[32]  Herwig Baier,et al.  Visual Prey Capture in Larval Zebrafish Is Controlled by Identified Reticulospinal Neurons Downstream of the Tectum , 2005, The Journal of Neuroscience.

[33]  M. Wullimann,et al.  The zebrafish brain: a neuroanatomical comparison with the goldfish , 1996, Anatomy and Embryology.

[34]  M. Wullimann,et al.  BrdU-, neuroD (nrd)- and Hu-studies reveal unusual non-ventricular neurogenesis in the postembryonic zebrafish forebrain , 2002, Mechanisms of Development.

[35]  Stephen L. Johnson,et al.  nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. , 1999, Development.

[36]  R. Anadón,et al.  Neural connections of the pineal organ in the primitive bony fish Acipenser baeri: A carbocyanine dye tract‐tracing study , 1998, The Journal of comparative neurology.

[37]  D. Fisher,et al.  Involvement of Microphthalmia in the Inhibition of Melanocyte Lineage Differentiation and of Melanogenesis by Agouti Signal Protein* , 1998, The Journal of Biological Chemistry.

[38]  Ewert Jp,et al.  Neural correlates of key stimulus and releasing mechanism : a case study and two concepts , 1997 .

[39]  Dr. M. F. Wullimann,et al.  Neuroanatomy of the Zebrafish Brain , 1996, Birkhäuser Basel.

[40]  S. Easter,et al.  Development of the retinofugal projections in the embryonic and larval zebrafish (Brachydanio rerio) , 1994, The Journal of comparative neurology.

[41]  吉本 正美.  Cytoarchitecture, fiber connections, and ultrastructure of the nucleus pretectalis superficialis pars magnocellularis (PSm) in carp , 1994 .

[42]  Hironobu Ito,et al.  Cytoarchitecture, fiber connections, and ultrastructure of the nucleus pretectalis superficialis pars magnocellularis (PSm) in carp , 1993, The Journal of comparative neurology.

[43]  S. Yaxley,et al.  Sensory-specific satiety: Food-specific reduction in responsiveness of ventral forebrain neurons after feeding in the monkey , 1986, Brain Research.

[44]  P. Laming,et al.  Brain mechanisms of behaviour in lower vertebrates , 1983 .

[45]  R. Beauchamp,et al.  Visual responses of nucleus corticalis neurons in the perciform teleost, Northern Rock Bass (Ambloplites rupestris rupestris) , 1982, Brain Research.

[46]  J. Ewert,et al.  Neuroethology , 1980, Springer Berlin Heidelberg.

[47]  G. Savage,et al.  Effects of hypothalamic lesions on the food intake of the goldfish (Carassius auratus). , 1978, Brain, behavior and evolution.

[48]  E. T. Rolls,et al.  Hypothalamic neuronal responses associated with the sight of food , 1976, Brain Research.

[49]  E. Rolls,et al.  Effects of hunger on the responses of neurons in the lateral hypothalamus to the sight and taste of food , 1976, Experimental Neurology.

[50]  W. Pitts,et al.  What the Frog's Eye Tells the Frog's Brain , 1959, Proceedings of the IRE.

[51]  H. Barlow.  Summation and inhibition in the frog's retina , 1953, The Journal of physiology.

[52]  J. McKENDRICK,et al.  The Central Nervous System of Vertebrates , 1909, Nature.