Monosynaptic pathway from rat vibrissa motor cortex to facial motor neurons revealed by lentivirus-based axonal tracing

Journal of Neuroscience

Volumn 25, Issue 36, 2005, Pages 8250-8258

  Grinevich, Valery ^a   Brecht, Michael ^a,b   Osten, Pavel ^a  

^a MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Axonal tracing; Facial nucleus; GFP; Lentivirus; Motor neuron; Vibrissa motor cortex

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; SYNAPTOPHYSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; FACIAL NERVE NUCLEUS; LENTIVIRINAE; MONOSYNAPTIC PATHWAY; MOTOR CORTEX; NERVE ENDING; NERVE FIBER TRANSPORT; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD MOTONEURON; VIBRISSA;

ANIMALS; AXONS; ELECTRIC STIMULATION; FACE; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; LENTIVIRUS; MOTOR CORTEX; MOTOR NEURONS; MOVEMENT; PYRAMIDAL CELLS; RATS; SYNAPSES; VIBRISSAE;

EID: 24744451402     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2235-05.2005     Document Type: Article

References (62)

1. Alstermark B, Ogawa J, Isa T (2004) Lack of monosynaptic corticomotoneuronal EPSPs in rats: disynaptic EPSPs mediated via reticulospinal neurons and polysynaptic EPSPs via segmental interneurons. J Neurophysiol 91:1832-1839.
2. Berg RW, Kleinfeld D (2003) Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. J Neurophysiol 89:104-117.
3. Berod A, Hartman BK, Pujol JF (1981) Importance of fixation in immunohistochemistry: use of formaldehyde solutions at variable pH for the localization of tyrosine hydroxylase. J Histochem Cytochem 29:844-850.
4. Blömer U, Naldini L, Kafri T, Trono D, Verma IM, Gage FH (1997) Highly efficient and sustained gene transfer in adult neurons with a lentivirus vector. J Virol 71:6641-6649.
5. Bortoff GA, Strick PL (1993) Corticospinal terminations in two new-world primates: further evidence that corticomotoneuronal connections provide part of the neural substrate for manual dexterity. J Neurosci 13:5105-5118.
6. Brecht M, Preilowski B, Merzenich MM (1997) Functional architecture of the mystacial vibrissae. Behav Brain Res 84:81-97.
7. Brecht M, Schneider M, Sakmann B, Margrie TW (2004a) Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 427:704-710.
8. Brecht M, Krauss A, Muhammad S, Sinai-Esfahani L, Bellanca S, Margrie TW (2004b) Organization of rat vibrissa motor cortex and adjacent areas according to cytoarchitectonics, microstimulation, and intracellular stimulation of identified cells. J Comp Neurol 479:360-373.
9. Carvell GE, Simons DJ (1990) Biometric analyses of vibrissal tactile discrimination in the rat. J Neurosci 10:2638-2648.
10. Costello MB, Fragaszy DM (1988) Prehension in Cebus and Saimiri: I. Grip type and hand preference. Am J Primatol 15:235-245.
11. De Paola V, Arber S, Caroni P (2003) AMPA receptors regulate dynamic equilibrium of presynaptic terminals in mature hippocampal networks. Nat Neurosci 6:491-500.
12. Desmaris N, Bosch A, Salaun C, Petit C, Prevost MC, Tordo N, Perrin P, Schwartz O, de Rocquigny H, Heard JM (2001) Production and neurotropism of lentivirus vectors pseudotyped with lyssavirus envelope glycoproteins. Mol Ther 4:149-156.
13. Dittgen T, Nimmerjahn A, Komai S, Licznerski P, Waters J, Margrie TW, Helmchen F, Denk W, Brecht M, Osten P (2004) Lentivirus-based genetic manipulations of cortical neurons and their optical and electrophysiological monitoring in vivo. Proc Natl Acad Sci USA 101:18206-18211.
14. Dörfl J (1982) The musculature of the mystacial vibrissae of the white mouse. J Anat 135:147-154.
15. Elger CE, Speckmann EJ, Caspers H, Janzen RW (1977) Cortico-spinal connections in the rat. I. Monosynaptic and polysynaptic responses of cervical motoneurons to epicortical stimulation. Exp Brain Res 28:385-404.
16. Friauf E (1986) Morphology of motoneurons in different subdivisions of the rat facial nucleus stained intracellularly with horseradish peroxidase. J Comp Neurol 253:231-241.
17. Guic-Robles E, Valdivieso C, Guajardo G (1989) Rats can learn a roughness discrimination using only their vibrissal system. Behav Brain Res 31:285-289.
18. Haiss F, Schwarz C (2005) Spatial segregation of different modes of movement control in the whisker representation of rat primary motor cortex. J Neurosci 25:1579-1587.
19. Hall RD, Lindholm EP (1974) Organization of motor and somatosensory neocortex in the albino rat. Brain Res 66:23-28.
20. Harvey MA, Bermejo R, Zeigler HP (2001) Discriminative whisking in the head-fixed rat: optoelectronic monitoring during tactile detection and discrimination tasks. Somatosens Mot Res 18:211-222.
21. Hattox A, Li Y, Keller A (2003) Serotonin regulates rhythmic whisking. Neuron 39:343-352.
22. Hattox AM, Priest CA, Keller A (2002) Functional circuitry involved in the regulation of whisker movements. J Comp Neurol 442:266-276.
23. Hrabetova S, Nicholson C (2002) Do electron micrographs underestimate gaps between brain cells? Soc Neurosci Abstr 28:505.517.
24. Izraeli R, Porter LL (1995) Vibrissal motor cortex in the rat: connections with the barrel field. Exp Brain Res 104:41-54.
25. Jenny AB, Saper CB (1987) Organization of the facial nucleus and corticofacial projection in the monkey: a reconsideration of the upper motor neuron facial palsy. Neurology 37:930-939.
26. Jin TE, Witzemann V, Brecht M (2004) Fiber types of the intrinsic whisker muscle and whisking behavior. J Neurosci 24:3386-3393.
27. Jürgens U, Alipour M (2002) A comparative study on the corticohypoglossal connections in primates, using biotin dextranamine. Neurosci Lett 328:245-248.
28. Kay MA, Glorioso JC, Naldini L (2001) Viral vectors for gene therapy: the art of turning infectious agents into vehicles of therapeutics. Nat Med 7:33-40.
29. Klein BG, Rhoades RW (1985) Representation of whisker follicle intrinsic musculature in the facial motor nucleus of the rat. J Comp Neurol 232:55-69.
30. Kleinfeld D, Berg RW, O'Connor SM (1999) Anatomical loops and their electrical dynamics in relation to whisking by rat. Somatosens Mot Res 16:69-88.
31. Kootstra NA, Verma IM (2003) Gene therapy with viral vectors. Annu Rev Pharmacol Toxicol 43:413-439.
32. Krupa DJ, Matell MS, Brisben AJ, Oliveira LM, Nicolelis MA (2001) Behavioral properties of the trigeminal somatosensory system in rats performing whisker-dependent tactile discriminations. J Neurosci 21:5752-5763.
33. Kuypers HG (1958a) Corticobular connexions to the pons and lower brainstem in man: an anatomical study. Brain 81:364-388.
34. Kuypers HG (1958b) Some projections from the peri-central cortex to the pons and lower brain stem in monkey and chimpanzee. J Comp Neurol 110:221-255.
35. Kuypers HG (1982) A new look at the organization of the motor system. Prog Brain Res 57:381-403.
36. Lee KJ, Woolsey TA (1975) A proportional relationship between peripheral innervation density and cortical neuron number in the somatosensory system of the mouse. Brain Res 99:349-353.
37. Lemon RN, Bennett KMB, Werner W (1991) The cortico-motor substrate for skilled movements of the primate hand. In: Tutorials on motor neuroscience (Stelmach GE, Requin J, eds), pp 477-495. Holland: Kluwer Academic.
38. Liang FY, Moret V, Wiesendanger M, Rouiller EM (1991) Corticomotoneuronal connections in the rat: evidence from double-labeling of motoneurons and corticospinal axon arborizations. J Comp Neurol 311:356-366.
39. Liposits Z, Sherman D, Phelix C, Paull WK (1986) A combined light and electron microscopic immunocytochemical method for the simultaneous localization of multiple tissue antigens. Tyrosine hydroxylase immunoreactive innervation of corticotropin releasing factor synthesizing neurons in the paraventricular nucleus of the rat. Histochemistry 85:95-106.
40. Lois C, Hong EJ, Pease S, Brown EJ, Baltimore D (2002) Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295:868-872.
41. Miyashita E, Keller A, Asanuma H (1994) Input-output organization of the rat vibrissal motor cortex. Exp Brain Res 99:223-232.
42. Mogoseanu D, Smith AD, Bolam JP (1994) Monosynaptic innervation of facial motoneurones by neurones of the parvicellular reticular formation. Exp Brain Res 101:427-438.
43. Morecraft RJ, Louie JL, Herrick JL, Stilwell-Morecraft KS (2001) Cortical innervation of the facial nucleus in the non-human primate: a new interpretation of the effects of stroke and related subtotal brain trauma on the muscles of facial expression. Brain 124:176-208.
44. Morecraft RJ, Stilwell-Morecraft KS, Rossing WR (2004) The motor cortex and facial expression: new insights from neuroscience. Neurologist 10:235-249.
45. Nakata T, Terada S, Hirokawa N (1998) Visualization of the dynamics of synaptic vesicle and plasma membrane proteins in living axons. J Cell Biol 140:659-674.
46. Naldini L, Blömer U, Gallay P, Ory D, Mulligan R, Gage FH, Verma IM, Trono D (1996) In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272:263-267.
47. Nguyen QT, Kleinfeld D (2005) Positive feedback in a brainstem tactile sensorimotor loop. Neuron 45:447-457.
48. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. San Diego: Academic.
49. Porter R, Lemon R (1995) Corticospinal function and voluntary movement. In: Monographs of the physiological society. Gloucestershire, UK: Clarendon.
50. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208-212.
51. Sachdev RN, Sato T, Ebner FF (2002) Divergent movement of adjacent whiskers. J Neurophysiol 87:1440-1448.
52. Sachdev RN, Berg RW, Champney G, Kleinfeld D, Ebner FF (2003) Unilateral vibrissa contact: changes in amplitude but not timing of rhythmic whisking. Somatosens Mot Res 20:163-169.
53. Semba K, Egger MD (1986) The facial "motor" nerve of the rat: control of vibrissal movement and examination of motor and sensory components. J Comp Neurol 247:144-158.
54. Senba E, Tohyama M (1983) Leucine-enkephalin-containing neuron system in the facial nucleus of the rat with special reference to its fine structure. Brain Res 274:17-23.
55. Van Harreveld A (1972) The extracellular space in the vertebrate central nervous system. In: The structure and function of nervous tissue (Bourne GH, ed), pp 447-511. New York: Academic.
56. Welker WI (1964) Analysis of sniffing of the albino rat. Behaviour 22:223-244.
57. Wiedenmann B, Franke WW (1985) Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell 41:1017-1028.
58. Wimmer VC, Nevian T, Kuner T (2004) Targeted in vivo expression of proteins in the calyx of Held. Pflügers Arch 449:319-333.
59. Wineski LE (1985) Facial morphology and vibrissal movement in the golden hamster. J Morphol 183:199-217.
60. Wree A, Lutz B, Thole U (1992) Volumes of the cytoarchitectonic areas in the rat cerebral cortex. J Hirnforsch 33:545-548.
61. Yang HW, Lemon RN (2003) An electron microscopic examination of the corticospinal projection to the cervical spinal cord in the rat: lack of evidence for cortico-motoneuronal synapses. Exp Brain Res 149:458-469.
62. Zaborszky L, Heimer L (1989) Combinations of tracer techniques, especially HRP and PHA-L, with transmitter identification for correlated light and electron microscopic studies. In: Neuroanatomical tract tracing methods 2 plenum (Heimer L, Zaborszky L, eds), pp 49-96. New York: Plenum.