Development of oculomotor circuitry independent of hox3 genes

Nature Communications

Volumn 5, Issue , 2014, Pages

  Ma, Leung Hang ^a   Grove, Charlotte L ^a   Baker, Robert ^a  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; CYPRINID; EYE; GENE EXPRESSION; MOVEMENT; NEUROLOGY;

ARTICLE; CONNECTOME; EYE MOVEMENT; EYE MOVEMENT CONTROL; GENE EXPRESSION; HOX 3 GENE; HOX GENE; MOTONEURON; NEUROMERE; NONHUMAN; OCULOMOTOR CIRCUIT; OCULOMOTOR NERVE; RHOMBENCEPHALON; ZEBRA FISH; ANIMAL; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMEOBOX; METABOLISM; NERVE TRACT;

HOMEODOMAIN PROTEIN; HOXA3 PROTEIN, ZEBRAFISH; HOXB3A PROTEIN, ZEBRAFISH; ZEBRAFISH PROTEIN;

ANIMALS; EYE MOVEMENTS; GENE KNOCKDOWN TECHNIQUES; GENES, HOMEOBOX; HOMEODOMAIN PROTEINS; NEURAL PATHWAYS; RHOMBENCEPHALON; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84903287547     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5221     Document Type: Article

References (68)

1. Tumpel, S., Wiedemann, L. M. & Krumlauf, R. Hox genes and segmentation of the vertebrate hindbrain. Curr. Top. Dev. Biol. 88, 103-137 (2009).
2. Dasen, J. S. & Jessell, T. M. Hox networks and the origins of motor neuron diversity. Curr. Top. Dev. Biol. 88, 169-200 (2009).
3. Guo, T. et al. An evolving NGF-Hoxd1 signaling pathway mediates development of divergent neural circuits in vertebrates. Nat. Neurosci. 14, 31-36 (2011).
4. Oury, F. et al. Hoxa2-and rhombomere-dependent development of the mouse facial somatosensory map. Science 313, 1408-1413 (2006). (Pubitemid 44360263)
5. Gavalas, A., Davenne, M., Lumsden, A., Chambon, P. & Rijli, F. M. Role of Hoxa-2 in axon pathfinding and rostral hindbrain patterning. Development 124, 3693-3702 (1997). (Pubitemid 27482966)
6. Jung, H. et al. Global control of motor neuron topography mediated by the repressive actions of a single hox gene. Neuron 67, 781-796 (2010).
7. Narita, Y. & Rijli, F. M. Hox genes in neural patterning and circuit formation in the mouse hindbrain. Curr. Top. Dev. Biol. 88, 139-167 (2009).
8. Hale, M. E., Kheirbek, M. A., Schriefer, J. E. & Prince, V. E. Hox gene misexpression and cell-specific lesions reveal functionality of homeotically transformed neurons. J. Neurosci. 24, 3070-3076 (2004). (Pubitemid 38405754)
9. del Toro, E. D. et al. Generation of a novel functional neuronal circuit in Hoxa1 mutant mice. J. Neurosci. 21, 5637-5642 (2001).
10. Di Bonito, M. et al. Assembly of the auditory circuitry by a Hox genetic network in the mouse brainstem. PLoS Genet. 9, e1003249 (2013).
11. Bianco, I. H. et al. The tangential nucleus controls a gravito-inertial vestibulo-ocular reflex. Curr. Biol. 22, 1285-1295 (2012).
12. Beck, J. C., Gilland, E., Tank, D. W. & Baker, R. Quantifying the ontogeny of optokinetic and vestibuloocular behaviors in zebrafish, medaka, and goldfish. J. Neurophysiol. 92, 3546-3561 (2004). (Pubitemid 39506331)
13. Buttner, U. & Buttner-Ennever, J. A. Present concepts of oculomotor organization. Prog. Brain Res. 151, 1-42 (2006). (Pubitemid 41420826)
14. Shinoda, Y., Sugiuchi, Y., Takahashi, M. & Izawa, Y. Neural substrate for suppression of omnipause neurons at the onset of saccades. Ann. N. Y. Acad. Sci. 1233, 100-106 (2011).
15. Scudder, C. A., Kaneko, C. S. & Fuchs, A. F. The brainstem burst generator for saccadic eye movements: a modern synthesis. Exp. Brain Res. 142, 439-462 (2002). (Pubitemid 34169833)
16. Moens, C. B. & Prince, V. E. Constructing the hindbrain: insights from the zebrafish. Dev. Dyn. 224, 1-17 (2002). (Pubitemid 34464928)
17. Soshnikova, N. Hox genes regulation in vertebrates. Dev. Dyn. 243, 49-58 (2013).
18. Philippidou, P. & Dasen, J. S. Hox genes: choreographers in neural development, architects of circuit organization. Neuron 80, 12-34 (2013).
19. Schoonheim, P. J., Arrenberg, A. B., Del Bene, F. & Baier, H. Optogenetic localization and genetic perturbation of saccade-generating neurons in zebrafish. J. Neurosci. 30, 7111-7120 (2010).
20. Beck, J. C., Rothnie, P., Straka, H., Wearne, S. L. & Baker, R. Precerebellar hindbrain neurons encoding eye velocity during vestibular and optokinetic behavior in the goldfish. J. Neurophysiol. 96, 1370-1382 (2006). (Pubitemid 44371528)
21. Escudero, M., de la Cruz, R. R. & Delgado-Garcia, J. M. A physiological study of vestibular and prepositus hypoglossi neurones projecting to the abducens nucleus in the alert cat. J. Physiol. 458, 539-560 (1992). (Pubitemid 23024609)
22. Pastor, A. M., Torres, B., Delgado-Garcia, J. M. & Baker, R. Discharge characteristics of medial rectus and abducens motoneurons in the goldfish. J. Neurophysiol. 66, 2125-2140 (1991).
23. Moens, C. B., Cordes, S. P., Giorgianni, M. W., Barsh, G. S. & Kimmel, C. B. Equivalence in the genetic control of hindbrain segmentation in fish and mouse. Development 125, 381-391 (1998). (Pubitemid 28102647)
24. Moens, C. B., Yan, Y. L., Appel, B., Force, A. G. & Kimmel, C. B. valentino: a zebrafish gene required for normal hindbrain segmentation. Development 122, 3981-3990 (1996).
25. Gilland, E. & Baker, R. Conservation of neuroepithelial and mesodermal segments in the embryonic vertebrate head. Acta. Anat. (Basel) 148, 110-123 (1993). (Pubitemid 24013457)
26. Cooke, J. et al. Eph signalling functions downstream of Val to regulate cell sorting and boundary formation in the caudal hindbrain. Development 128, 571-580 (2001). (Pubitemid 32229599)
27. Manzanares, M. et al. Independent regulation of initiation and maintenance phases of Hoxa3 expression in the vertebrate hindbrain involve auto-and crossregulatory mechanisms. Development 128, 3595-3607 (2001). (Pubitemid 32962726)
28. Prince, V. E., Moens, C. B., Kimmel, C. B. & Ho, R. K. Zebrafish hox genes: expression in the hindbrain region of wild-type and mutants of the segmentation gene, valentino. Development 125, 393-406 (1998). (Pubitemid 28102648)
29. Manzanares, M. et al. Segmental regulation of Hoxb-3 by kreisler. Nature 387, 191-195 (1997). (Pubitemid 27209435)
30. Hernandez, R. E., Rikhof, H. A., Bachmann, R. & Moens, C. B. vhnf1 integrates global RA patterning and local FGF signals to direct posterior hindbrain development in zebrafish. Development 131, 4511-4520 (2004). (Pubitemid 39409692)
31. Sadl, V. S., Sing, A., Mar, L., Jin, F. & Cordes, S. P. Analysis of hindbrain patterning defects caused by the kreisler(enu) mutation reveals multiple roles of Kreisler in hindbrain segmentation. Dev. Dyn. 227, 134-142 (2003). (Pubitemid 36523333)
32. McKay, I. J. et al. The kreisler mouse: a hindbrain segmentation mutant that lacks two rhombomeres. Development 120, 2199-2211 (1994). (Pubitemid 24232287)
33. Philippidou, P., Walsh, C. M., Aubin, J., Jeannotte, L. & Dasen, J. S. Sustained Hox5 gene activity is required for respiratory motor neuron development. Nat. Neurosci. 15, 1636-1644 (2012).
34. Bingham, S. M. et al. Multiple mechanisms mediate motor neuron migration in the zebrafish hindbrain. Dev. Neurobiol. 70, 87-99 (2010).
35. Guidato, S., Prin, F. & Guthrie, S. Somatic motoneurone specification in the hindbrain: the influence of somite-derived signals, retinoic acid and Hoxa3. Development 130, 2981-2996 (2003). (Pubitemid 36857245)
36. Gaufo, G. O., Thomas, K. R. & Capecchi, M. R. Hox3 genes coordinate mechanisms of genetic suppression and activation in the generation of branchial and somatic motoneurons. Development 130, 5191-5201 (2003). (Pubitemid 37369678)
37. Manzanares, M. et al. Conserved and distinct roles of kreisler in regulation of the paralogous Hoxa3 and Hoxb3 genes. Development 126, 759-769 (1999). (Pubitemid 29106182)
38. Manley, N. R. & Capecchi, M. R. Hox group 3 paralogous genes act synergistically in the formation of somitic and neural crest-derived structures. Dev. Biol. 192, 274-288 (1997). (Pubitemid 28066933)
39. Watari, N., Kameda, Y., Takeichi, M. & Chisaka, O. Hoxa3 regulates integration of glossopharyngeal nerve precursor cells. Dev. Biol. 240, 15-31 (2001). (Pubitemid 33141106)
40. Debowy, O. & Baker, R. Encoding of eye position in the goldfish horizontal oculomotor neural integrator. J. Neurophysiol. 105, 896-909 (2011).
41. Masseck, O. A. & Hoffmann, K. P. Comparative neurobiology of the optokinetic reflex. Ann. N. Y. Acad. Sci. 1164, 430-439 (2009).
42. Marsh, E. & Baker, R. Normal and adapted visuooculomotor reflexes in goldfish. J. Neurophysiol. 77, 1099-1118 (1997). (Pubitemid 27137013)
43. Mensh, B. D., Aksay, E., Lee, D. D., Seung, H. S. & Tank, D. W. Spontaneous eye movements in goldfish: oculomotor integrator performance, plasticity, and dependence on visual feedback. Vision Res. 44, 711-726 (2004). (Pubitemid 38125110)
44. Miri, A., Daie, K., Burdine, R. D., Aksay, E. & Tank, D. W. Regressionbased identification of behavior-encoding neurons during large-scale optical imaging of neural activity at cellular resolution. J. Neurophysiol. 105, 964-980 (2011).
45. Aksay, E. et al. Functional dissection of circuitry in a neural integrator. Nat. Neurosci. 10, 494-504 (2007). (Pubitemid 46494596)
46. Major, G. et al. Plasticity and tuning by visual feedback of the stability of a neural integrator. Proc. Natl Acad. Sci. USA 101, 7739-7744 (2004). (Pubitemid 38658099)
47. Aksay, E., Baker, R., Seung, H. S. & Tank, D. W. Anatomy and discharge properties of pre-motor neurons in the goldfish medulla that have eye-position signals during fixations. J. Neurophysiol. 84, 1035-1049 (2000). (Pubitemid 30655621)
48. Pastor, A. M., De la Cruz, R. R. & Baker, R. Eye position and eye velocity integrators reside in separate brainstem nuclei. Proc. Natl Acad. Sci. USA 91, 807-811 (1994). (Pubitemid 24041491)
49. Beck, J. C., Tank, D. W. & Baker, R. Ontogeny of persistent neural activity: Maturation of gaze holding in zebrafish. Abstract Viewer/Itinerary Planner. Washington DCSoc. for Neuroscience. Program No. 391.391 (2003).
50. Maklad, A. & Fritzsch, B. Development of vestibular afferent projections into the hindbrain and their central targets. Brain Res. Bull. 60, 497-510 (2003). (Pubitemid 36638314)
51. Chandrasekhar, A., Moens, C. B., Warren, Jr J. T., Kimmel, C. B. & Kuwada, J. Y. Development of branchiomotor neurons in zebrafish. Development 124, 2633-2644 (1997). (Pubitemid 27341763)
52. Gaufo, G. O., Wu, S. & Capecchi, M. R. Contribution of Hox genes to the diversity of the hindbrain sensory system. Development 131, 1259-1266 (2004). (Pubitemid 38443880)
53. Lacombe, J. et al. Genetic and functional modularity of Hox activities in the specification of limb-innervating motor neurons. PLoS Genet. 9, e1003184 (2013).
54. Isogai, S., Horiguchi, M. & Weinstein, B. M. The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development. Dev. Biol. 230, 278-301 (2001). (Pubitemid 32171423)
55. Green, M. H., Curet, O. M., Patankar, N. A. & Hale, M. E. Fluid dynamics of the larval zebrafish pectoral fin and the role of fin bending in fluid transport. Bioinspir. Biomim. 8, 016002 (2013).
56. Wullimann, M. F. et al. The long adventurous journey of rhombic lip cells in jawed vertebrates: a comparative developmental analysis. Front. Neuroanat. 5, 27 (2011).
57. Kinkhabwala, A. et al. A structural and functional ground plan for neurons in the hindbrain of zebrafish. Proc. Natl Acad. Sci. USA 108, 1164-1169 (2011).
58. Volkmann, K., Chen, Y. Y., Harris, M. P., Wullimann, M. F. & Koster, R. W. The zebrafish cerebellar upper rhombic lip generates tegmental hindbrain nuclei by long-distance migration in an evolutionary conserved manner. J. Comp. Neurol. 518, 2794-2817 (2010).
59. Ma, L. H., Punnamoottil, B., Rinkwitz, S. & Baker, R. Mosaic hoxb4a neuronal pleiotropism in zebrafish caudal hindbrain. PLoS ONE 4, e5944 (2009).
60. Ma, L. H., Gilland, E., Bass, A. H. & Baker, R. Ancestry of motor innervation to pectoral fin and forelimb. Nat. Commun. 1, 49 (2010).
61. Higashijima, S., Hotta, Y. & Okamoto, H. Visualization of cranial motor neurons in live transgenic zebrafish expressing green fluorescent protein under the control of the islet-1 promoter/enhancer. J. Neurosci. 20, 206-218 (2000). (Pubitemid 30220508)
62. Moens, C. B. & Selleri, L. Hox cofactors in vertebrate development. Dev. Biol. 291, 193-206 (2006).
63. Fritzsch, B. et al. Evolution and development of the tetrapod auditory system: an organ of Corti-centric perspective. Evol. Dev. 15, 63-79 (2013).
64. Fritzsch, B. Evolution of the vestibulo-ocular system. Otolaryngol. Head Neck Surg. 119, 182-192 (1998). (Pubitemid 28425604)
65. Graf, W. Spatial coordination of compensatory eye movements in vertebrates: form and function. Acta Biol. Hung. 39, 279-290 (1988).
66. Straka, H. & Baker, R. Vestibular blueprint in early vertebrates. Front. Neural Circuits 7, 182 (2013).
67. Baker, R. & Gilland, E. in Acquisition of Motor Behavior in Vertebrates (eds Bloedel, J. R., Ebner, T. J. & Wise, S. P.) 29-55 (MIT Press, 1996).
68. Jing, L., Gordon, L. R., Shtibin, E. & Granato, M. Temporal and spatial requirements of unplugged/MuSK function during zebrafish neuromuscular development. PLoS ONE 5, e8843 (2010).