The whisking rhythm generator: A novel mammalian network for the generation of movement

Journal of Neurophysiology

Volumn 97, Issue 3, 2007, Pages 2148-2158

  Cramer, Nathan P ^a   Li, Ying ^a   Keller, Asaf ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EVOKED CORTICAL RESPONSE; MOTOR NERVE CONDUCTION; MOTOR PERFORMANCE; MOVEMENT (PHYSIOLOGY); NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; RHYTHM; SEROTONINERGIC SYSTEM; VIBRISSA;

ANIMALS; ANIMALS, NEWBORN; BRAIN STEM; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; DRUG INTERACTIONS; ELECTRIC STIMULATION; ELECTROMYOGRAPHY; MEMBRANE POTENTIALS; MOTOR NEURONS; MOVEMENT; NERVE NET; PATCH-CLAMP TECHNIQUES; PERIODICITY; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN; SEROTONIN AGONISTS; SODIUM CHANNEL BLOCKERS; TETRODOTOXIN; VIBRISSAE;

EID: 33947144603     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01187.2006     Document Type: Article

References (58)

1. Arshavsky YI, Deliagina TG, Orlovsky GN. Pattern generation. Curr Opin Neurobiol 7: 781-789, 1997.
2. Azmitia E, Gannon P. The ultrastructural localization of serotonin immunoreactivity in myelinated and unmyelinated axons within the medial forebrain bundle of rat and monkey. J Neurosci 3: 2083-2090, 1983.
3. Bellintani-Guardia B, Schweizer M, Herbert H. Analysis of projections from the cochlear nucleus to the lateral paragigantocellular reticular nucleus in the rat. Cell Tissue Res 283: 493-505, 1996.
4. Berg RW, Kleinfeld D. Vibrissa movement elicited by rhythmic electrical microstimulation to motor cortex in the aroused rat mimics exploratory whisking. J Neurophysiol 90: 2950-2963, 2003.
5. Bowker R, Abbott L. Quantitative re-evaluation of descending serotonergic and non-serotonergic projections from the medulla of the rodent: evidence for extensive co-existence of serotonin and peptides in the same spinally projecting neurons but not from the nucleus raphe magnus. Brain Res 512: 15-25, 1990.
6. Brecht M, Preilowski B, Merzenich MM. Functional architecture of the mystacial vibrissae. Behav Brain Res 84: 81-97, 1997.
7. Carvell GE, Miller SA, Simons DJ. The relationship of vibrissal motor cortex unit activity to whisking in the awake rat. Somatosens Mot Res 13: 115-127, 1996.
8. Carvell G, Simons DJ. Biometric analyses of vibrissal tactile discrimination in the rat. J Neurosci 10: 2638-2648, 1990.
9. Castro-Alamancos MA. Vibrissa myoclonus (rhythmic retractions) driven by resonance of excitatory networks in motor cortex. J Neurophysiol 96: 1691-1698, 2006.
10. Connors BW, Long MA. Electrical synapses in the mammalian brain. Annu Rev Neurosci 27: 393-418, 2004.
11. Courville J. The nucleus of the facial nerve: The relation between cellular groups and peripheral branches of the nerve. Brain Res 1: 338-354, 1966.
12. Cramer NP, Keller A. Cortical control of a whisking central pattern generator. J Neurophysiol 96: 209-217, 2006.
13. Darnall RA, Harris MB, Gill WH, Hoffman JM, Brown JW, Niblock MM. Inhibition of serotonergic neurons in the nucleus paragigantocellularis lateralis fragments sleep and decreases rapid eye movement sleep in the piglet: implications for sudden infant death syndrome. J Neurosci 25: 8322-8332, 2005.
14. De-Miguel FF, Trueta C. Synaptic and extrasynaptic secretion of serotonin. Cell Mol Neurobiol 25: 297-312, 2005.
15. Fanardjian VV, Manvelyan LR, Kasabyan SA. Mechanisms regulating the activity of facial nucleus motoneurons. I. Antidromic activation. Neuroscience 9: 815-822, 1983.
16. Friedberg MH, Lee SM, Ebner FF. Modulation of receptive field properties of thalamic somatosensory neurons by the depth of anesthesia. J Neurophysiol 81: 2243-2252, 1999.
17. Friedman WA, Jones LM, Cramer NP, Kwegyir-Afful EE, Zeigler HP, Keller A. Anticipatory activity of motor cortex in relation to rhythmic whisking. J Neurophysiol 95: 1274-1277, 2006.
18. Gao P, Bermejo B, Zeigler P. Whisker deafferentation and rodent whisking patterns: behavioral evidence for a central pattern generator. J Neurosci 21: 5374-5380, 2001.
19. Gao P, Hattox AM, Jones LM, Keller A, Zeigler HP. Whisker motor cortex ablation and whisker movement patterns. Somatosens Mot Res 20: 191-198, 2003.
20. Graziano M. The organization of behavioral repertoire in motor cortex. Annu Rev Neurosci 29: 105-134, 2006.
21. 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 25: 8250-8258, 2005.
22. Haiss F, Schwarz C. Spatial segregation of different modes of movement control in the whisker representation of rat primary motor cortex. J Neurosci 25: 1579-1587, 2005.
23. Harvey PJ, Li X, Li Y, Bennett DJ. 5-HT2 receptor activation facilitates a persistent sodium current and repetitive firing in spinal motoneurons of rats with and without chronic spinal cord injury. J Neurophysiol 96: 1158-1170, 2006a.
24. Harvey PJ, Li X, Li Y, Bennett DJ. Endogenous monoamine receptor activation is essential for enabling persistent sodium currents and repetitive firing in rat spinal motoneurons. J Neurophysiol 96: 1171-1186, 2006b.
25. Hattox AM, Li Y, Keller A. Serotonin regulates rhythmic whisking. Neuron 39: 342-352, 2003.
26. Hattox AM, Priest CA, Keller A. Functional circuitry involved in the regulation of whisker movements. J Comp Neurol 442: 266-276, 2002.
27. Heckman CJ, Gorassini MA, Bennett DJ. Persistent inward currents in motoneuron dendrites: implications for motor output. Muscle Nerve 31: 135-156, 2005.
28. Heckman CJ, Kuo JJ, Johnson MD. Synaptic integration in motoneurons with hyper-excitable dendrites. Can J Physiol Pharmacol 82: 549-555, 2004.
29. Heckman CJ, Lee RH, Brownstone RM. Hyperexcitable dendrites in motoneurons and their neuromodulatory control during motor behavior. Trends Neurosci 26: 688-695, 2003.
30. Hounsgaard J, Hultborn H, Jespersen B, Kiehn O. Bistability of alphamotoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan. J Physiol 405: 345-367, 1988.
31. Hounsgaard J, Kiehn O. Serotonin-induced bistability of turtle motoneurons caused by a nifedipine-sensitive calcium plateau potential. J Physiol 414: 265-282, 1989.
32. Hsiao CF, Del Negro CA, Trueblood PR, Chandler SH. Ionic basis for serotonin-induced bistable membrane properties in guinea pig trigeminal motoneurons. J Neurophysiol 79: 2847-2856, 1998.
33. Hsiao C, Trueblood P, Levine M, Chandler S. Multiple effects of serotonin on membrane properties of trigeminal motoneurons in vitro. J Neurophysiol 77: 2910-2924, 1997.
34. Hunt PN, Gust J, McCabe AK, Bosma MM. Primary role of the serotonergic midline system in synchronized spontaneous activity during development of the embryonic mouse hindbrain. J Neurobiol 66: 1239-1252, 2006.
35. Kiehn O, Tresch MC. Gap junctions and motor behavior. Trends Neurosci 25: 108-115, 2002.
36. Klein BG, Rhoades RW. Representation of whisker follicle intrinsic musculature in the facial motor nucleus of the rat. J Comp Neurol 232: 55-69, 1985.
37. Lee RH, Heckman CJ. Bistability in spinal motoneurons in vivo: systematic variations in persistent inward currents. J Neurophysiol 80: 583-593, 1998.
38. Lovick TA. The behavioral repertoire of precollicular decerebrate rats. J Physiol 224: 4-6, 1972.
39. McCall RB, Aghajanian GK. Serotonergic facilitation of facial motoneuron excitation. Brain Res 169: 11-27, 1979.
40. Orlovksy GN, Deliagina TG, Grillner S. Neuronal Control of Locomotion: From Mollusc to Man. New York: Oxford, 1999.
41. Perrier JF, Hounsgaard J. 5-HT2 receptors promote plateau potentials in turtle spinal motoneurons by facilitating an L-type calcium current. J Neurophysiol 89: 954-959, 2003.
42. Powers RK, Binder MD. Input-output functions of mammalian motoneurons. Rev Physiol Biochem Pharmacol 143: 137-263, 2001.
43. Powers RK, Binder MD. Persistent sodium and calcium currents in rat hypoglossal motoneurons. J Neurophysiol 89: 615-624, 2003.
44. Prather JF, Powers RK, Cope TC. Amplification and linear summation of synaptic effects on motoneuron firing rate. J Neurophysiol 85: 43-53, 2001.
45. Rekling JC, Funk GD, Bayliss DA, Dong XW, Feldman JL. Synaptic central of motoneuronal excitability. Physiol Rev 80: 767-852, 2000.
46. Rohlmann A, Laskawi R, Hofer A, Dobo E, Dermietzel R, Wolff JR. Facial nerve lesions lead to increased immunostaining of the astrocytic gap junction protein (connexin 43) in the corresponding facial nucleus of rats. Neurosci Lett 154: 206-108, 1993.
47. Sachdev RNS, Sato T, Ebner FF. Divergent movement of adjacent whiskers. J Neurophysiol 87: 1440-1448, 2002.
48. Schwindt PC, Crill WE. Properties of a persistent inward current in normal and TEA-injected motoneurons. J Neurophysiol 43: 1700-1724, 1980.
49. Schwindt PC, Crill WE. Factors influencing motoneuron rhythmic firing: results from a voltage-clamp study. J Neurophysiol 48: 875-890, 1982.
50. Semba K, Egger MD. The facial "motor" nerve of the rat: control of vibrissal movement and examination of motor and sensory components. J Comp Neurol 247: 144-158, 1986.
51. Semba K, Komisaruk BR. Neural substrates of two different rhythmical vibrissal movements in the rat. Neuroscience 12: 761-774, 1984.
52. Stein PSG, Grillner S, Selverston AL, Stuart DG. Neurons, Networks, and Motor Behavior. Cambridge, MA: The MIT Press, 1997.
53. Towal RB, Hartmann MJ. Right-left asymmetries in the whisking behavior of rats anticipate head movements. J Neurosci 26: 8838-8846, 2006.
54. Tresch MC, Kiehn O. Motor coordination without action potentials in the mammalian spinal cord. Nat Neurosci 3: 593-599, 2000.
55. Vincent SB. The function of the vibrissae in the behavior of the white rat. Behav Monogr 1: 7-86, 1912.
56. Welker WI. Analysis of sniffing of the albino rat. Behavior 22: 223-244, 1964.
57. Wu N, Enomoto A, Tanaka S, Hsiao CF, Nykamp DQ, Izhikevich E, Chandler SH. Persistent sodium currents in mesencephalic v neurons participate in burst generation and control of membrane excitability. J Neurophysiol 93: 2710-2722, 2005.
58. Zhang L, Sykes KT, Buhler AV, Hammond DL. Electrophysiological heterogeneity of spinally projecting serotonergic and nonserotonergic neurons in the rostral ventromedial medulla. J Neurophysiol 95: 1853-1863, 2006.