Descending Control of Swim Posture by a Midbrain Nucleus in Zebrafish

The reticular formation in the brainstem controls motor output via axonal projections to the hindbrain and spinal cord. It remains unclear how individual groups of brainstem neurons contribute to specific motor functions. Here, we investigate the behavioral role of the nucleus of the medial longitudinal fasciculus (nMLF), a small group of reticulospinal neurons in the zebrafish midbrain. Calcium imaging revealed that nMLF activity is correlated with bouts of swimming. Optogenetic stimulation of neurons in the left or right nMLF activates the posterior hypaxial muscle and produces a graded ipsilateral tail deflection. Unilateral ablation of a subset of nMLF cells biases the tail position to the intact side during visually evoked swims, while sparing other locomotor maneuvers. We conclude that activity in the nMLF provides postural control of tail orientation and thus steers the direction of swimming. Our studies provide an example of fine-grained modularity of descending motor control in vertebrates.

[1]  Kevin L. Briggman,et al.  Multifunctional pattern-generating circuits. , 2008, Annual review of neuroscience.

[2]  K. Uematsu,et al.  Central Mechanisms Underlying Fish Swimming , 2007, Brain, Behavior and Evolution.

[3]  E. Ball,et al.  Initiation and modulation of flight by a single giant interneuron in the cercal system of the locust , 2004, Naturwissenschaften.

[4]  Masayuki Yoshida,et al.  Artificial control of swimming in goldfish by brain stimulation: Confirmation of the midbrain nuclei as the swimming center , 2009, Neuroscience Letters.

[5]  A. Miyawaki,et al.  An optical marker based on the UV-induced green-to-red photoconversion of a fluorescent protein , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[6]  S. Grillner,et al.  Cellular bases of a vertebrate locomotor system–steering, intersegmental and segmental co-ordination and sensory control , 2002, Brain Research Reviews.

[7]  Ethan Gahtan,et al.  Visually guided injection of identified reticulospinal neurons in zebrafish: A survey of spinal arborization patterns , 2003, The Journal of comparative neurology.

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

[9]  S. Mori Integration of posture and locomotion in acute decerebrate cats and in awake, freely moving cats , 1987, Progress in Neurobiology.

[10]  S. Grillner,et al.  Activity of reticulospinal neurons during locomotion in the freely behaving lamprey. , 2000, Journal of neurophysiology.

[11]  M. Sirota,et al.  Stimulation of the mesencephalic locomotor region elicits controlled swimming in semi‐intact lampreys , 2000, The European journal of neuroscience.

[12]  Tatiana G Deliagina,et al.  Comparative neurobiology of postural control , 2002, Current Opinion in Neurobiology.

[13]  A. Ménard,et al.  Initiation of locomotion in lampreys , 2008, Brain Research Reviews.

[14]  Christel Genoud,et al.  Analyzing the structure and function of neuronal circuits in zebrafish , 2013, Front. Neural Circuits.

[15]  O. Kiehn Locomotor circuits in the mammalian spinal cord. , 2006, Annual review of neuroscience.

[16]  E. Bizzi,et al.  Modules in the brain stem and spinal cord underlying motor behaviors. , 2011, Journal of neurophysiology.

[17]  C. Wiersma Giant nerve fiber system of the crayfish; a contribution to comparative physiology of synapse. , 1947, Journal of neurophysiology.

[18]  E. Bizzi,et al.  Article history: , 2005 .

[19]  Emilio Bizzi,et al.  Coordination and localization in spinal motor systems , 2002, Brain Research Reviews.

[20]  Kristen E. Severi,et al.  Control of visually guided behavior by distinct populations of spinal projection neurons , 2008, Nature Neuroscience.

[21]  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.

[22]  Herwig Baier,et al.  Genetic and optical targeting of neural circuits and behavior—zebrafish in the spotlight , 2009, Current Opinion in Neurobiology.

[23]  Karel Svoboda,et al.  ScanImage: Flexible software for operating laser scanning microscopes , 2003, Biomedical engineering online.

[24]  B. W. Peterson,et al.  Reticulospinal connections with limb and axial motoneurons , 1979, Experimental Brain Research.

[25]  Yen-Hong Kao,et al.  Imaging the Functional Organization of Zebrafish Hindbrain Segments during Escape Behaviors , 1996, Neuron.

[26]  Shik Ml,et al.  Control of walking and running by means of electric stimulation of the midbrain , 1966 .

[27]  Sten Grillner,et al.  Biological Pattern Generation: The Cellular and Computational Logic of Networks in Motion , 2006, Neuron.

[28]  D. O'Malley,et al.  Locomotor repertoire of the larval zebrafish: swimming, turning and prey capture. , 2000, The Journal of experimental biology.

[29]  W. K. Metcalfe,et al.  Brain neurons which project to the spinal cord in young larvae of the zebrafish , 1982, The Journal of comparative neurology.

[30]  Herwig Baier,et al.  Optical control of zebrafish behavior with halorhodopsin , 2009, Proceedings of the National Academy of Sciences.

[31]  Florian Engert,et al.  Adaptive Locomotor Behavior in Larval Zebrafish , 2011, Front. Syst. Neurosci..

[32]  Aristides B. Arrenberg,et al.  Optogenetic Localization and Genetic Perturbation of Saccade-Generating Neurons in Zebrafish , 2010, The Journal of Neuroscience.

[33]  S. Grillner,et al.  Comparison of the motor effects of individual vestibulo- and reticulospinal neurons on dorsal and ventral myotomes in lamprey. , 2003, Journal of neurophysiology.

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

[35]  J. Fetcho,et al.  Laser Ablations Reveal Functional Relationships of Segmental Hindbrain Neurons in Zebrafish , 1999, Neuron.

[36]  T. Deliagina,et al.  Responses of reticulospinal neurons in intact lamprey to pitch tilt. , 2002, Journal of neurophysiology.

[37]  W. K. Metcalfe,et al.  Noninvasive recording of the Mauthner neurone action potential in larval zebrafish. , 1982, The Journal of experimental biology.

[38]  E. Gahtan,et al.  Evidence for a widespread brain stem escape network in larval zebrafish. , 2002, Journal of neurophysiology.

[39]  S. Brenner,et al.  The neural circuit for touch sensitivity in Caenorhabditis elegans , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  M. L. Shik,et al.  [Control of walking and running by means of electric stimulation of the midbrain]. , 1966, Biofizika.

[41]  R. Bryson-Richardson,et al.  Met and Hgf signaling controls hypaxial muscle and lateral line development in the zebrafish , 2004, Development.

[42]  Timothy W. Dunn,et al.  Spinal Projection Neurons Control Turning Behaviors in Zebrafish , 2013, Current Biology.

[43]  S. Lockery,et al.  Distributed processing of sensory information in the leech. II. Identification of interneurons contributing to the local bending reflex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  Chie Satou,et al.  Hindbrain V2a Neurons in the Excitation of Spinal Locomotor Circuits during Zebrafish Swimming , 2013, Current Biology.

[45]  N. Sankrithi,et al.  Activation of a multisensory, multifunctional nucleus in the zebrafish midbrain during diverse locomotor behaviors , 2010, Neuroscience.

[46]  Grigori N. Orlovsky,et al.  Control of spatial orientation in a mollusc , 1998, Nature.

[47]  P. Stein,et al.  Modular Organization of Turtle Spinal Interneurons during Normal and Deletion Fictive Rostral Scratching , 2002, The Journal of Neuroscience.

[48]  Movement- and behavioral state-dependent activity of pontine reticulospinal neurons , 2012, Neuroscience.

[49]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[50]  J. -. Wu,et al.  Neuronal activity during different behaviors in Aplysia: a distributed organization? , 1994, Science.

[51]  S. Grillner,et al.  Differential effects of the reticulospinal system on locomotion in lamprey. , 1998, Journal of neurophysiology.

[52]  Stimulation-induced setting of postural muscle tone in the decerebrate rat , 1991, Brain Research.

[53]  K. Deisseroth,et al.  Millisecond-timescale, genetically targeted optical control of neural activity , 2005, Nature Neuroscience.

[54]  Herwig Baier,et al.  Lamina-specific axonal projections in the zebrafish tectum require the type IV collagen Dragnet , 2007, Nature Neuroscience.