Cerebellar premotor output neurons collateralize to innervate the cerebellar cortex

Journal of Comparative Neurology

Volumn 523, Issue 15, 2015, Pages 2254-2271

  Houck, Brenda D ^a   Person, Abigail L ^a  

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

Author keywords

AB_10051818; AB_10054551; AB_10307; AB_10566289; AB_143165; AB_2315774; AB_305564; AB_528480; AB_91937; Corollary discharge; Efference copy; Interposed; motor coordination; Purkinje; RRIDs: AB_2315383

Indexed keywords

CRE RECOMBINASE; BIOTIN; BIOTINYLATED DEXTRAN AMINE; DEXTRAN; NEURONAL TRACT TRACER; NEUROTENSIN RECEPTOR; NEUROTENSIN TYPE 1 RECEPTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; BRAIN MAPPING; CEREBELLUM CORTEX; CEREBELLUM NUCLEUS; CONNECTOME; CONTROLLED STUDY; ELECTRON MICROSCOPY; FEEDBACK SYSTEM; IMMUNOHISTOCHEMISTRY; MOLECULAR IMAGING; MOSSY FIBER; MOUSE; NERVOUS SYSTEM FUNCTION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RED NUCLEUS; THALAMUS VENTRAL NUCLEUS; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CEREBELLUM; CONFOCAL MICROSCOPY; CYTOLOGY; GENETICS; METABOLISM; NERVE CELL; NERVE TRACT; NEUROANATOMICAL TRACT TRACING; TRANSGENIC MOUSE;

ANIMALS; BIOTIN; CEREBELLUM; DEXTRANS; IMMUNOHISTOCHEMISTRY; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; NEURAL PATHWAYS; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; NEURONAL TRACT-TRACERS; NEURONS; RECEPTORS, NEUROTENSIN; RED NUCLEUS; VENTRAL THALAMIC NUCLEI;

EID: 84939272551     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23787     Document Type: Article

References (79)

1. Angaut P, Bowsher D. 1970. Ascending projections of the medial cerebellar (fastigial) nucleus: an experimental study in the cat. Brain Res 24:49-68.
2. Angaut P, Guilbaud G, Reymond MC. 1968. An electrophysiological study of the cerebellar projections to the nucleus ventralis lateralis of thalamus in the cat. I. Nuclei fastigii et inerpositus. J Comp Neurol 134:9-20.
3. Angaut P, Batini C, Billard JM, Daniel H. 1986. The cerebellorubral projection in the rat: retrograde anatomical study. Neurosci Lett 68:63-68.
4. Angaut P, Compoint C, Buisseret-Delmas C, Batini C. 1996. Synaptic connections of Purkinje cell axons with nucleocortical neurones in the cerebellar medial nucleus of the rat. Neurosci Res 26:345-348.
5. Batini C, Compoint C, Buisseret-Delmas C, Daniel H, Guegan M. 1992. Cerebellar nuclei and the nucleocortical projections in the rat: retrograde tracing coupled to GABA and glutamate immunohistochemistry. J Comp Neurol 315:74-84.
6. Bell CC. 1981. An efference copy which is modified by reafferent input. Science 214:450-453.
7. Bell CC, Grant K. 1989. Corollary discharge inhibition and preservation of temporal information in a sensory nucleus of mormyrid electric fish. J Neurosci 9:1029-1044.
8. Bell CC, Han V, Sawtell NB. 2008. Cerebellum-like structures and their implications for cerebellar function. Annu Rev Neurosci 31:1-24.
9. Bellebaum C, Daum I, Koch B, Schwarz M, Hoffmann K-P. 2005. The role of the human thalamus in processing corollary discharge. Brain J Neurol 128:1139-1154.
10. Brodal A, Drablos PA. 1963. Two types of mossy fiber terminals in the cerebellum and their regional distribution. J Comp Neurol 121:173-187.
11. Buckley K, Kelly RB. 1985. Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. J Cell Biol 100:1284-1294.
12. Buisseret-Delmas C, Angaut P. 1993. The cerebellar olivo-corticonuclear connections in the rat. Prog Neurobiol 40:63-87.
13. Chan-Palay V. 1977. Cerebellar dentate nucleus: organization, cytology and transmitters. Berlin: Springer.
14. Chan-Palay V, Palay SL, Wu JY. 1979. Gamma-aminobutyric acid pathways in the cerebellum studied by retrograde and anterograde transport of glutamic acid decarboxylase antibody after in vivo injections. Anat Embryol (Berl) 157:1-14.
15. Clarke PG. 1977. Some visual and other connections to the cerebellum of the pigeon. J Comp Neurol 174:535-552.
16. Crapse TB, Sommer MA. 2008. Corollary discharge across the animal kingdom. Nat Rev Neurosci 9:587-600.
17. Daniel H, Billard JM, Angaut P, Batini C. 1987. The interposito-rubrospinal system. Anatomical tracing of a motor control pathway in the rat. Neurosci Res 5:87-112.
18. Dietrichs E. 1983. The cerebellar corticonuclear and nucleocortical projections in the cat as studied with anterograde and retrograde transport of horseradish peroxidase. V. The posterior lobe vermis and the flocculo-nodular lobe. Anat Embryol (Berl) 167:449-462.
19. Dietrichs E, Walberg F. 1979. The cerebellar corticonuclear and nucleocortical projections in the cat as studied with anterograde and retrograde transport of horseradish peroxidase. I. The paramedian lobule. Anat Embryol (Berl) 158:13-39.
20. Dietrichs E, Walberg F. 1980. The cerebellar corticonuclear and nucleocortical projections in the cat as studied with anterograde and retrograde transport of horseradish peroxidase. II. Lobulus simplex, crus I and II. Anat Embryol (Berl) 161:83-103.
21. Faull RL, Carman JB. 1978. The cerebellofugal projections in the brachium conjunctivum of the rat I. The contralateral ascending pathway. J Comp Neurol 178:495-517.
22. Franklin DW, Wolpert DM. 2011. Computational mechanisms of sensorimotor control. Neuron 72:425-442.
23. Fu Y, Tvrdik P, Makki N, Paxinos G, Watson C. 2011. Precerebellar cell groups in the hindbrain of the mouse defined by retrograde tracing and correlated with cumulative Wnt1-cre genetic labeling. Cerebellum 10:570-584.
24. Gebre SA, Reeber SL, Sillitoe RV. 2012. Parasagittal compartmentation of cerebellar mossy fibers as revealed by the patterned expression of vesicular glutamate transporters VGLUT1 and VGLUT2. Brain Struct Funct 217:165-180.
25. Gonzalez-Joekes J, Schreurs BG. 2012. Anatomical characterization of a rabbit cerebellar eyeblink premotor pathway using pseudorabies and identification of a local modulatory network in anterior interpositus. J Neurosci 32:12472-12487.
26. Gould BB, Graybiel AM. 1976. Afferents to the cerebellar cortex in the cat: evidence for an intrinsic pathway leading from the deep nuclei to the cortex. Brain Res 110:601-611.
27. Green AM, Meng H, Angelaki DE. 2007. A reevaluation of the inverse dynamic model for eye movements. J Neurosci 27:1346-1355.
28. Guthrie BL, Porter JD, Sparks DL. 1983. Corollary discharge provides accurate eye position information to the oculomotor system. Science 221:1193-1195.
29. Haines DE. 1989. HRP study of cerebellar corticonuclear-nucleocortical topography of the dorsal culminate lobule-lobule V-in a prosimian primate (Galago): with comments on nucleocortical cell types. J Comp Neurol 282:274-292.
30. Haines DE, Pearson JC. 1979. Cerebellar corticonuclear - nucleocortical topography: a study of the tree shrew (Tupaia) paraflocculus. J Comp Neurol 187:745-758.
31. Hámori J, Takács J. 1989. Two types of GABA-containing axon terminals in cerebellar glomeruli of cat: an immunogold-EM study. Exp Brain Res 74:471-479.
32. Harris KM, Perry E, Bourne J, Feinberg M, Ostroff L, Hurlburt J. 2006. Uniform serial sectioning for transmission electron microscopy. J Neurosci 26:12101-12103.
33. Heiney SA, Kim J, Augustine GJ, Medina JF. 2014. Precise control of movement kinematics by optogenetic inhibition of Purkinje cell activity. J Neurosci 34:2321-2330.
34. Hendelman WJ, Marshall KC. 1980. Axonal projection patterns visualized with horseradish peroxidase in organized cultures of cerebellum. Neuroscience 5:1833-1846.
35. Hesslow G. 1994. Inhibition of classically conditioned eyeblink responses by stimulation of the cerebellar cortex in the decerebrate cat. J Physiol 476:245-256.
36. Houck BD, Person AL. 2014. Cerebellar loops: a review of the nucleocortical pathway. Cerebellum 13:378-385.
37. Huang C-C, Sugino K, Shima Y, Guo C, Bai S, Mensh BD, Nelson SB, Hantman AW. 2013. Convergence of pontine and proprioceptive streams onto multimodal cerebellar granule cells. eLife 2:e00400.
38. Huisman AM, Kuypers HG, Ververs B. 1983. Retrograde neuronal labeling of cells of origin of descending brainstem pathways in rat using SITS as a retrograde tracer. Brain Res 289:305-310.
39. Husson Z, Rousseau CV, Broll I, Zeilhofer HU, Dieudonné S. 2014. Differential GABAergic and glycinergic inputs of inhibitory interneurons and purkinje cells to principal cells of the cerebellar nuclei. J Neurosci 34:9418-9431.
40. Ito M. 1984. The modifiable neuronal network of the cerebellum. Jpn J Physiol 34:781-792.
41. Kalil K. 1981. Projections of the cerebellar and dorsal column nuclei upon the thalamus of the rhesus monkey. J Comp Neurol 195:25-50.
42. Kawato M, Gomi H. 1992. The cerebellum and VOR/OKR learning models. Trends Neurosci 15:445-453.
43. Kolston J, Apps R, Trott JR. 1995. A combined retrograde tracer and GABA-immunocytochemical study of the projection from nucleus interpositus posterior to the posterior lobe C2 zone of the cat cerebellum. Eur J Neurosci 7:926-933.
44. Lisberger SG. 2009. Internal models of eye movement in the floccular complex of the monkey cerebellum. Neuroscience 162:763-776.
45. Mauk MD, Thompson RF. 1987. Retention of classically conditioned eyelid responses following acute decerebration. Brain Res 403:89-95.
46. McCrea RA, Bishop GA, Kitai ST. 1978. Morphological and electrophysiological characteristics of projection neurons in the nucleus interpositus of the cat cerebellum. J Comp Neurol 181:397-419.
47. Miall RC, Weir DJ, Wolpert DM, Stein JF. 1993. Is the cerebellum a smith predictor? J Mot Behav 25:203-216.
48. Mohr C, Roberts PD, Bell CC. 2003. The mormyromast region of the mormyrid electrosensory lobe. I. Responses to corollary discharge and electrosensory stimuli. J Neurophysiol 90:1193-1210.
49. Oberdick J, Sillitoe RV. 2011. Cerebellar zones: history, development, and function. Cerebellum 10:301-306.
50. Ohyama T, Nores WL, Murphy M, Mauk MD. 2003. What the cerebellum computes. Trends Neurosci 26:222-227.
51. Päällysaho J, Sugita S, Noda H. 1990. Cerebellar corticonuclear and nucleocortical projections in the vermis of posterior lobe of the rat as studied with anterograde and retrograde transport of WGA-HRP. Neurosci Res 8:158-178.
52. Palay SL, Chan-Palay V. 1974. Cerebellar cortex: cytology and organization. Berlin, Heidelberg: Springer.
53. Paxinos G, Franklin KBJ. 2008. The mouse brain in stereotaxic coordinates, 3rd ed. Amsterdam: Elsevier Academic Press.
54. Payne JN. 1983. The cerebellar nucleo-cortical projection in the rat studied by the retrograde fluorescent double-labelling method. Brain Res 271:141-144.
55. Proville RD, Spolidoro M, Guyon N, Dugué GP, Selimi F, Isope P, Popa D, Léna C. 2014. Cerebellum involvement in cortical sensorimotor circuits for the control of voluntary movements. Nat Neurosci 17:1233-1239.
56. Provini L, Redman S, Strata P. 1968. Mossy and climbing fibre organization on the anterior lobe of the cerebellum activated by forelimb and hindlimb areas of the sensorimotor cortex. Exp Brain Res 6:216-233.
57. Raymond JL, Lisberger SG, Mauk MD. 1996. The cerebellum: a neuronal learning machine? Science 272:1126-1131.
58. Rivlin PK, Raymond PA. 1987. Use of osmium tetroxide-potassium ferricyanide in reconstructing cells from serial ultrathin sections. J Neurosci Methods 20:23-33.
59. Rothermel M, Brunert D, Zabawa C, Díaz-Quesada M, Wachowiak M. 2013. Transgene expression in target-defined neuron populations mediated by retrograde infection with adeno-associated viral vectors. J Neurosci 33:15195-15206.
60. Ruigrok TJH, Teune TM. 2014. Collateralization of cerebellar output to functionally distinct brainstem areas. A retrograde, non-fluorescent tracing study in the rat. Front Syst Neurosci 8:23.
61. Shadmehr R, Krakauer JW. 2008. A computational neuroanatomy for motor control. Exp Brain Res 185:359-381.
62. Shinoda Y, Futami T, Mitoma H, Yokota J. 1988. Morphology of single neurones in the cerebello-rubrospinal system. Behav Brain Res 28:59-64.
63. Sillitoe RV, Benson MA, Blake DJ, Hawkes R. 2003. Abnormal dysbindin expression in cerebellar mossy fiber synapses in the mdx mouse model of Duchenne muscular dystrophy. J Neurosci 23:6576-6585.
64. Simat M, Parpan F, Fritschy J-M. 2007. Heterogeneity of glycinergic and gabaergic interneurons in the granule cell layer of mouse cerebellum. J Comp Neurol 500:71-83.
65. Sommer MA, Wurtz RH. 2008. Brain circuits for the internal monitoring of movements. Annu Rev Neurosci 31:317-338.
66. Sperry RW. 1950. Neural basis of the spontaneous optokinetic response produced by visual inversion. J Comp Physiol Psychol 43:482-489.
67. Steinmetz AB, Freeman JH. 2014. Localization of the cerebellar cortical zone mediating acquisition of eyeblink conditioning in rats. Neurobiol Learn Mem 114C:148-154.
68. Stone LS, Lisberger SG. 1990. Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple spikes. J Neurophysiol 63:1241-1261.
69. Teune TM, van der Burg J, Ruigrok TJ. 1995. Cerebellar projections to the red nucleus and inferior olive originate from separate populations of neurons in the rat: a non-fluorescent double labeling study. Brain Res 673:313-319.
70. Teune TM, van der Burg J, van der Moer J, Voogd J, Ruigrok TJ. 2000. Topography of cerebellar nuclear projections to the brain stem in the rat. Prog Brain Res 124:141-172.
71. Tolbert DL, Bantli H, Bloedel JR. 1976. Anatomical and physiological evidence for a cerebellar nucleo-cortical projection in the cat. Neuroscience 1:205-217.
72. Tolbert DL, Bantli H, Bloedel JR. 1977. The intracerebellar nucleocortical projection in a primate. Exp Brain Res 30:425-434.
73. Tolbert DL, Bantli H, Bloedel JR. 1978. Multiple branching of cerebellar efferent projections in cats. Exp Brain Res 31:305-316.
74. Tolbert D, Kultas-Ilinsky K, Ilinsky I. 1980. EM-autoradiography of cerebellar nucleocortical terminals in the cat. Anat Embryol (Berl) 161:215-223.
75. Trott JR, Apps R, Armstrong DM. 1990. Topographical organisation within the cerebellar nucleocortical projection to the paravermal cortex of lobule Vb/c in the cat. Exp Brain Res 80:415-428.
76. Uusisaari M, Knöpfel T. 2010. GlyT2+ neurons in the lateral cerebellar nucleus. Cerebellum 9:42-55.
77. Wolpert DM. 1997. Computational approaches to motor control. Trends Cogn Sci 1:209-216.
78. Wolpert DM, Miall RC, Kawato M. 1998. Internal models in the cerebellum. Trends Cogn Sci 2:338-347.
79. Zeilhofer HU, Studler B, Arabadzisz D, Schweizer C, Ahmadi S, Layh B, Bösl MR, Fritschy J-M. 2005. Glycinergic neurons expressing enhanced green fluorescent protein in bacterial artificial chromosome transgenic mice. J Comp Neurol 482:123-141.