New Modules Are Added to Vibrissal Premotor Circuitry with the Emergence of Exploratory Whisking

Neuron

Volumn 77, Issue 2, 2013, Pages 346-360

  Takatoh, Jun ^a   Nelson, Anders ^a   Zhou, Xiang ^b   Bolton, M McLean ^c   Ehlers, Michael D ^d   Arenkiel, Benjamin R ^e   Mooney, Richard ^a   Wang, Fan ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c MAX PLANCK FLORIDA INSTITUTE FOR NEUROSCIENCE   (United States)

^d PFIZER INC   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; BRAIN STEM; CELL LABELING; CONTROLLED STUDY; COORDINATION; EXPLORATORY BEHAVIOR; LATERAL PARAGIGANTOCELLULARIS; MOTONEURON; MOTOR CORTEX; MOUSE; MUSCLE INNERVATION; NERVE CELL NETWORK; NERVE FIBER; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RABIES VIRUS; SYNAPTIC TRANSMISSION; VIBRISSA; VIBRISSA FACIAL MOTOR NEURON;

ANIMALS; ANIMALS, NEWBORN; EXPLORATORY BEHAVIOR; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR CORTEX; NERVE NET; SOMATOSENSORY CORTEX; VIBRISSAE;

EID: 84872704327     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2012.11.010     Document Type: Article

References (58)

1. Arenkiel B.R., Ehlers M.D. Molecular genetics and imaging technologies for circuit-based neuroanatomy. Nature 2009, 461:900-907.
2. Arenkiel B.R., Hasegawa H., Yi J.J., Larsen R.S., Wallace M.L., Philpot B.D., Wang F., Ehlers M.D. Activity-induced remodeling of olfactory bulb microcircuits revealed by monosynaptic tracing. PLoS ONE 2011, 6:e29423.
3. Aronov D., Andalman A.S., Fee M.S. A specialized forebrain circuit for vocal babbling in the juvenile songbird. Science 2008, 320:630-634.
4. Ashwell K.W., Watson C.R. The development of facial motoneurones in the mouse-neuronal death and the innervation of the facial muscles. J. Embryol. Exp. Morphol. 1983, 77:117-141.
5. Berg R.W., Kleinfeld D. Vibrissa movement elicited by rhythmic electrical microstimulation to motor cortex in the aroused rat mimics exploratory whisking. J. Neurophysiol. 2003, 90:2950-2963.
6. Berg R.W., Friedman B., Schroeder L.F., Kleinfeld D. Activation of nucleus basalis facilitates cortical control of a brain stem motor program. J. Neurophysiol. 2005, 94:699-711.
7. Brecht M., Krauss A., Muhammad S., Sinai-Esfahani L., Bellanca S., Margrie T.W. Organization of rat vibrissa motor cortex and adjacent areas according to cytoarchitectonics, microstimulation, and intracellular stimulation of identified cells. J. Comp. Neurol. 2004, 479:360-373.
8. Callaway E.M. Transneuronal circuit tracing with neurotropic viruses. Curr. Opin. Neurobiol. 2008, 18:617-623.
9. Carvell G.E., Miller S.A., Simons D.J. The relationship of vibrissal motor cortex unit activity to whisking in the awake rat. Somatosens. Mot. Res. 1996, 13:115-127.
10. Diamond M.E., von Heimendahl M., Knutsen P.M., Kleinfeld D., Ahissar E. 'Where' and 'what' in the whisker sensorimotor system. Nat. Rev. Neurosci. 2008, 9:601-612.
11. Dominici N., Ivanenko Y.P., Cappellini G., d'Avella A., Mondì V., Cicchese M., Fabiano A., Silei T., Di Paolo A., Giannini C., et al. Locomotor primitives in newborn babies and their development. Science 2011, 334:997-999.
12. Donoghue J.P., Parham C. Afferent connections of the lateral agranular field of the rat motor cortex. J. Comp. Neurol. 1983, 217:390-404.
13. Dörfl J. The musculature of the mystacial vibrissae of the white mouse. J. Anat. 1982, 135:147-154.
14. Dörfl J. The innervation of the mystacial region of the white mouse: A topographical study. J. Anat. 1985, 142:173-184.
15. Dutschmann M., Herbert H. The Kölliker-Fuse nucleus gates the postinspiratory phase of the respiratory cycle to control inspiratory off-switch and upper airway resistance in rat. Eur. J. Neurosci. 2006, 24:1071-1084.
16. Dutschmann M., Mörschel M., Kron M., Herbert H. Development of adaptive behaviour of the respiratory network: implications for the pontine Kolliker-Fuse nucleus. Respir. Physiol. Neurobiol. 2004, 143:155-165.
17. Etessami R., Conzelmann K.K., Fadai-Ghotbi B., Natelson B., Tsiang H., Ceccaldi P.E. Spread and pathogenic characteristics of a G-deficient rabies virus recombinant: an in vitro and in vivo study. J. Gen. Virol. 2000, 81:2147-2153.
18. Ezure K. Synaptic connections between medullary respiratory neurons and considerations on the genesis of respiratory rhythm. Prog. Neurobiol. 1990, 35:429-450.
19. Gao P., Bermejo R., Zeigler H.P. Whisker deafferentation and rodent whisking patterns: behavioral evidence for a central pattern generator. J. Neurosci. 2001, 21:5374-5380.
20. Gerber R.J., Wilks T., Erdie-Lalena C. Developmental milestones: motor development. Pediatr. Rev. 2010, 31:267-276. quiz 277.
21. Grant R.A., Mitchinson B., Prescott T.J. The development of whisker control in rats in relation to locomotion. Dev. Psychobiol. 2012, 54:151-168.
22. Gray P.A., Janczewski W.A., Mellen N., McCrimmon D.R., Feldman J.L. Normal breathing requires preBötzinger complex neurokinin-1 receptor-expressing neurons. Nat. Neurosci. 2001, 4:927-930.
23. Grinevich V., Brecht M., Osten P. Monosynaptic pathway from rat vibrissa motor cortex to facial motor neurons revealed by lentivirus-based axonal tracing. J. Neurosci. 2005, 25:8250-8258.
24. Hattox A., Li Y., Keller A. Serotonin regulates rhythmic whisking. Neuron 2003, 39:343-352.
25. Hattox A.M., Priest C.A., Keller A. Functional circuitry involved in the regulation of whisker movements. J. Comp. Neurol. 2002, 442:266-276.
26. Hill D.N., Bermejo R., Zeigler H.P., Kleinfeld D. Biomechanics of the vibrissa motor plant in rat: rhythmic whisking consists of triphasic neuromuscular activity. J. Neurosci. 2008, 28:3438-3455.
27. Hill D.N., Curtis J.C., Moore J.D., Kleinfeld D. Primary motor cortex reports efferent control of vibrissa motion on multiple timescales. Neuron 2011, 72:344-356.
28. Huber D., Gutnisky D.A., Peron S., O'Connor D.H., Wiegert J.S., Tian L., Oertner T.G., Looger L.L., Svoboda K. Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 2012, 484:473-478.
29. Immelman K. Song development in the zebra finch and other estrildid finches. Bird Vocalizations 1969, 61-77. Cambridge University Press, Cambridge, UK. R.A. Hinde (Ed.).
30. Isokawa-Akesson M., Komisaruk B.R. Difference in projections to the lateral and medial facial nucleus: anatomically separate pathways for rhythmical vibrissa movement in rats. Exp. Brain Res. 1987, 65:385-398.
31. Kelly R.M., Strick P.L. Rabies as a transneuronal tracer of circuits in the central nervous system. J. Neurosci. Methods 2000, 103:63-71.
32. Klein B.G., Rhoades R.W. Representation of whisker follicle intrinsic musculature in the facial motor nucleus of the rat. J. Comp. Neurol. 1985, 232:55-69.
33. Kleinfeld D., Ahissar E., Diamond M.E. Active sensation: insights from the rodent vibrissa sensorimotor system. Curr. Opin. Neurobiol. 2006, 16:435-444.
34. Kuhl P.K., Meltzoff A.N. Infant vocalizations in response to speech: vocal imitation and developmental change. J. Acoust. Soc. Am. 1996, 100:2425-2438.
35. Landers M., Philip Zeigler H. Development of rodent whisking: trigeminal input and central pattern generation. Somatosens. Mot. Res. 2006, 23:1-10.
36. Li C.X., Waters R.S. Organization of the mouse motor cortex studied by retrograde tracing and intracortical microstimulation (ICMS) mapping. Can. J. Neurol. Sci. 1991, 18:28-38.
37. Matyas F., Sreenivasan V., Marbach F., Wacongne C., Barsy B., Mateo C., Aronoff R., Petersen C.C. Motor control by sensory cortex. Science 2010, 330:1240-1243.
38. Mitchinson B., Martin C.J., Grant R.A., Prescott T.J. Feedback control in active sensing: rat exploratory whisking is modulated by environmental contact. Proc. Biol. Sci. 2007, 274:1035-1041.
39. Mooney R. Synaptic basis for developmental plasticity in a birdsong nucleus. J. Neurosci. 1992, 12:2464-2477.
40. Mooney R., Rao M. Waiting periods versus early innervation: the development of axonal connections in the zebra finch song system. J. Neurosci. 1994, 14:6532-6543.
41. O'Connor D.H., Clack N.G., Huber D., Komiyama T., Myers E.W., Svoboda K. Vibrissa-based object localization in head-fixed mice. J. Neurosci. 2010, 30:1947-1967.
42. Osakada F., Mori T., Cetin A.H., Marshel J.H., Virgen B., Callaway E.M. New rabies virus variants for monitoring and manipulating activity and gene expression in defined neural circuits. Neuron 2011, 71:617-631.
43. Petreanu L., Huber D., Sobczyk A., Svoboda K. Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat. Neurosci. 2007, 10:663-668.
44. Petreanu L., Mao T., Sternson S.M., Svoboda K. The subcellular organization of neocortical excitatory connections. Nature 2009, 457:1142-1145.
45. Sachdev R.N., Berg R.W., Champney G., Kleinfeld D., Ebner F.F. Unilateral vibrissa contact: changes in amplitude but not timing of rhythmic whisking. Somatosens. Mot. Res. 2003, 20:163-169.
46. Sellien H., Eshenroder D.S., Ebner F.F. Comparison of bilateral whisker movement in freely exploring and head-fixed adult rats. Somatosens. Mot. Res. 2005, 22:97-114.
47. Semba K., Egger M.D. The facial " motor" nerve of the rat: control of vibrissal movement and examination of motor and sensory components. J. Comp. Neurol. 1986, 247:144-158.
48. Smith J.C., Ellenberger H.H., Ballanyi K., Richter D.W., Feldman J.L. Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 1991, 254:726-729.
49. Smith J.C., Abdala A.P., Rybak I.A., Paton J.F. Structural and functional architecture of respiratory networks in the mammalian brainstem. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2009, 364:2577-2587.
50. Stepien A.E., Tripodi M., Arber S. Monosynaptic rabies virus reveals premotor network organization and synaptic specificity of cholinergic partition cells. Neuron 2010, 68:456-472.
51. Tan W., Janczewski W.A., Yang P., Shao X.M., Callaway E.M., Feldman J.L. Silencing preBötzinger complex somatostatin-expressing neurons induces persistent apnea in awake rat. Nat. Neurosci. 2008, 11:538-540.
52. Towal R.B., Hartmann M.J. Right-left asymmetries in the whisking behavior of rats anticipate head movements. J. Neurosci. 2006, 26:8838-8846.
53. Ugolini G. Specificity of rabies virus as a transneuronal tracer of motor networks: transfer from hypoglossal motoneurons to connected second-order and higher order central nervous system cell groups. J. Comp. Neurol. 1995, 356:457-480.
54. Wallace P.S., Whishaw I.Q. Independent digit movements and precision grip patterns in 1-5-month-old human infants: hand-babbling, including vacuous then self-directed hand and digit movements, precedes targeted reaching. Neuropsychologia 2003, 41:1912-1918.
55. Welker W.I. Analysis of sniffing of the albino rats. Behaviour 1964, 22:223-244.
56. Wickersham I.R., Finke S., Conzelmann K.K., Callaway E.M. Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat. Methods 2007, 4:47-49.
57. Wickersham I.R., Lyon D.C., Barnard R.J., Mori T., Finke S., Conzelmann K.K., Young J.A., Callaway E.M. Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron 2007, 53:639-647.
58. Wineski L.E. Facial morphology and vibrissal movement in the golden hamster. J. Morphol. 1985, 183:199-217.