Hierarchy of orofacial rhythms revealed through whisking and breathing

Nature

Volumn 497, Issue 7448, 2013, Pages 205-210

  Moore, Jeffrey D ^a   Deschênes, Martin ^b   Furuta, Takahiro ^c   Huber, Daniel ^a,d   Smear, Matthew C ^d   Demers, Maxime ^b   Kleinfeld, David ^a,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CENTRE DE RECHERCHE DE L INSTITUT UNIVERSITAIRE EN SANTÉ MENTALE DE QUÉBEC   (Canada)

^c KYOTO UNIVERSITY   (Japan)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^e UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANATOMY; HIERARCHICAL SYSTEM; NEUROLOGY; RESPIRATION; RODENT;

ANIMAL BEHAVIOR; ARTICLE; BRAIN FUNCTION; BREATHING; ELECTROPHYSIOLOGY; EXPLORATORY BEHAVIOR; FACE MUSCLE; MEDULLA OBLONGATA; MOTONEURON; NONHUMAN; OROFACIAL RHYTHM; PRIORITY JOURNAL; RESPIRATORY NERVE CELL; RHYTHM; SIGNAL PROCESSING; SNIFFING; VIBRISSA; WHISKING;

ANIMALS; BIOLOGICAL CLOCKS; FACE; FEMALE; HEAD MOVEMENTS; KAINIC ACID; MALE; MEDULLA OBLONGATA; MUSCLE, SKELETAL; RATS; RATS, LONG-EVANS; RESPIRATION; SMELL; VIBRISSAE;

RODENTIA;

EID: 84877774616     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12076     Document Type: Article

References (57)

1. Smith, J. C., Abdala, A. P. L., Rybak, I. A. & Paton, J. F. R. Structural and functional architecture of respiratory networks in the mammalian brainstem. Phil. Trans. R. Soc. B 364, 2577-2587 (2009).
2. Nakamura, Y. & Katakura, N. Generation of masticatory rhythm in the brainstem. Neurosci. Res. 23, 1-19 (1995).
3. Travers, J. B., Dinardo, L.A.& Karimnamazi, H. Motorandpremotormechanismsof licking. Neurosci. Biobehav. Rev. 21, 631-647 (1997).
4. Alheid, G. F.& McCrimmon, D. R. The chemical neuroanatomyof breathing. Respir. Physiol. Neurobiol. 164, 3-11 (2008).
5. Feldman, J. L.,DelNegro, C. A.&Gray, P. A.Understanding the rhythmof breathing: so near, yet so far. Annu. Rev. Physiol. 75, 423-452 (2013).
6. Garcia, A. J., Zanella, S., Koch, H., Doi, A.& Ramirez, J. M. Networks within networks: the neuronal control of breathing. Prog. Brain Res. 188, 31-50 (2011).
7. Welker, W. I. Analysis of sniffing of the albino rat. Behaviour 22, 223-244 (1964).
8. Brecht, M. & Freiwald, W. A. The many facets of facial interactions in mammals. Curr. Opin. Neurobiol. 22, 259-266 (2011).
9. Vincent, S. B. The function of the vibrissae in the behavior of the white rat. Behavior Monographs 1, 7-81 (1912).
10. Smith, J. C., Ellenberger, H. H., Ballanyi, K., Richter, D. W. & Feldman, J. L. Pre-Botzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254, 726-729 (1991).
11. Tan, W. et al. Silencing preBötzinger complex somatostatin- expressing neurons induces persistent apnea in awake rat. Nature Neurosci. 11, 538-540 (2008).
12. Dobbins, E. G. & Feldman, J. L. Brainstem network controlling descending drive to phrenic motoneurons in rat. J. Comp. Neurol. 347, 64-86 (1994).
13. Bieger, D. & Hopkins, D. A. Viscerotopic representation of the upper alimentary tract in the medulla oblongata in the rat: the nucleus ambiguus. J. Comp. Neurol. 262, 546-562 (1987).
14. Semba, K. & Komisaruk, B. R. Neural substrates of two different rhythmical vibrissal movements in the rat. Neuroscience 12, 761-774 (1984).
15. Berg, R. W. & Kleinfeld, D. Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. J. Neurophysiol. 89, 104-117 (2003).
16. Gao, P., Bermejo, R. & Zeigler, H. P. Vibrissa deaffentation and rodent whisking patterns: behavioral evidence for a central pattern generator. J. Neurosci. 21, 5374-5380 (2001).
17. Huangfu, D., Koshiya, N. & Guyenet, P. G. Central respiratory modulation of facial motoneurons in rats. Neurosci. Lett. 151, 224-228 (1993).
18. Onimaru, H., Kumagawa, Y. & Homma, I. Respiration-related rhythmic activity in the rostral medulla of newborn rats. J. Neurophysiol. 96, 55-61 (2006).
19. Lawson, E. E., Richter, D. W., Czyzyk-Krzeska, M. F., Bischoff, A. & Rudesill, R. C. Respiratory neuronal activity during apnea and other breathing patterns induced by laryngeal stimulation. J. Appl. Ohysiology 70, 2742-2749 (1991).
20. Fukuda, Y. & Honda, Y. Differences in respiratory neural activities between vagal (superior laryngeal), hypoglossal, and phrenic nerves in the anesthetized rat. Jpn. J. Physiol. 32, 387-398 (1982).
21. Ermentrout, G. B. & Kleinfeld, D. Traveling electrical waves in cortex: insights from phase dynamics and speculation on a computational role. Neuron 29, 33-44 (2001).
22. Sherrey, J. H. & Megirian, D. State dependence of upper airway respiratory motoneurons: functions of the cricothyroid and nasolabial muscles of the unanesthetized rat. Electroencephalogr. Clin. Neurophysiol. 43, 218-228 (1977).
23. Haidarliu, S., Golomb, D., Kleinfeld, D. & Ahissar, E. Dorsorostral snout muscles in the rat subserve coordinated movement for whisking and sniffing. Anat. Rec. 295, 1181-1191 (2012).
24. Dörfl, J. The musculature of the mystacial vibrissae of the white mouse. J. Anat. 135, 147-154 (1982).
25. 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. 28, 3438-3455 (2008).
26. Takatoh, J. et al. New modules are added to vibrissal premotor circuitry with the emergence of exploratory whisking. Neuron 77, 346-360 (2013).
27. 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. 65, 385-398 (1987).
28. Furuta, T. et al. Inhibitory gating of vibrissal inputs in the brainstem. J. Neurosci. 28, 1789-1797 (2008).
29. Chatterton, J. E. et al. Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 415, 793-798 (2002).
30. Pagliardini, S. et al. Active expiration induced by excitation of ventral medulla in adult anesthetized rats. J. Neurosci. 31, 2895-2905 (2011).
31. Klein, B. G. & Rhoades, R. The representation of whisker follicle intrinsic musculature in the facial motor nucleus of the rat. J. Comp. Neurol. 232, 55-69 (1985).
32. Gray, P. A. et al. Developmental origin of preBö tzinger complex respiratory neurons. J. Neurosci. 30, 14883-14895 (2010).
33. Bouvier, J. et al. Hindbrain interneurons and axon guidance signaling critical for breathing. Nature Neurosci. 13, 1066-1074 (2010).
34. Welzl, H. & Bures, J. Lick-synchronized breathing in rats. Physiol. Behav. 18, 751-753 (1977).
35. Koizumi, H. et al. Functional imaging, spatial reconstruction, and biophysical analysis of a respiratory motor circuit isolated in vitro. J. Neurosci. 28, 2353-2365 (2008).
36. Ono, T., Ishiwata, Y., Inaba, N., Kuroda, T. & Nakamura, Y. Modulation of the inspiratory-related activity of hypoglossal premotor neurons during ingestion and rejection in the decerebrate cat. J. Neurophysiol. 80, 48-58 (1998).
37. Travers, J. B., DiNardo, L. A. & Karimnamazi, H. Medullary reticular formation activity during ingestion and rejection in the awake rat. Exp. Brain Res. 130, 78-92 (2000).
38. Chen, Z., Travers,S. P.&Travers, J. B.Muscimol infusions in the brain stemreticular formation reversibly block ingestion in the awake rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, R1085-R1094 (2001).
39. DePuy, S. D., Kanbar, R., Coates, M. B., Stornetta, R. L. & Guyenet, P. G. Control of breathing by raphe obscurus serotonergic neurons in mice. J. Neurosci. 31, 1981-1990 (2011).
40. Doi, A. & Ramirez, J. M. Neuromodulation and the orchestration of the respiratory rhythm. Respir. Physiol. Neurobiol. 164, 96-104 (2008).
41. Hattox, A., Li, Y. & Keller, A. Serotonin regulates rhythmic whisking. Neuron 39, 343-352 (2003).
42. VanderMaelen, C. P. & Aghajanian, G. K. Intracellular studies showing modulation of facial motoneurone excitability by serotonin. Nature 287, 346-347 (1980).
43. Harish, O. & Golomb, D. Control of the firing patterns of vibrissa motoneurons by modulatory and phasic synaptic inputs: a modeling study. J. Neurophysiol. 103, 2684-2699 (2010).
44. Saito, Y., Ezure, K., Tanaka, I. & Osawa, M. Activity of neurons in ventrolateral respiratory groups during swallowing in decerebrate rats. Brain Dev. 25, 338-345 (2003).
45. Kleinfeld, D., Sachdev, R. N. S., Merchant, L. M., Jarvis, M. R. & Ebner, F. F. Adaptive filtering of vibrissa input in motor cortex of rat. Neuron 34, 1021-1034 (2002).
46. Lewis, T. L. Jr,Mao, T. & Svoboda,K.Myosin-dependent targeting of transmembrane proteins to neuronal dendrites. Nature Neurosci. 12, 568-576 (2009).
47. Uchida, N. & Mainen, Z. F.Speedandaccuracy of olfactory discriminationin the rat. Nature Neurosci. 6, 1224-1229 (2003).
48. Ganguly, K. & Kleinfeld, D. Goal-directed whisking behavior increases phaselocking between vibrissa movement and electrical activity in primary sensory cortex in rat. Proc. Natl Acad. Sci. USA 101, 12348-12353 (2004).
49. O'Connor, D. H. et al. Vibrissa-based object localization in head-fixed mice. J. Neurosci. 30, 1947-1967 (2010).
50. Shusterman, R., Smear, M. C., Koulakov, A. A. & Rinberg, D. Precise olfactory responses tile the sniff cycle. Nature Neurosci. 14, 1039-1044 (2011).
51. Knutsen, P. M.,Derdikman, D. & Ahissar, E. Tracking whisker and headmovements in unrestrained behaving rodents. J. Neurophysiol. 93, 2294-2301 (2005).
52. Hill, D. N.,Curtis, J. C.,Moore, J. D. & Kleinfeld,D.Primarymotor cortex reports efferent control of vibrissa position on multiple time scales. Neuron 72, 344-356 (2011).
53. Deschênes, M., Timofeeva, E. & Lavallee, P. The relay of high frequency sensory signals in the whisker-to-barreloid pathway. J. Neurosci. 23, 6778-6787 (2003).
54. Paxinos, G., Watson, C., Pennisi, M. & Topple, A. Bregma, lambda and the interaural midpoint in stereotaxic surgery with rats of different sex, strain and weight. J. Neurosci. Methods 13, 139-143 (1985).
55. Ghosh, S. et al. Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons. Nature 472, 217-220 (2011).
56. Paxinos, G. & Watson, C. The Rat Brain in Stereotaxic Coordinates 6thedn(Academic Press, 2007).
57. Ito, T. & Oliver, D. L. Origins of glutamatergic terminals in the inferior colliculus identified by retrograde transport and expression of VGLUT1 and VGLUT2 genes. Front. Neuroanat. 4, 135 (2010).