Three-dimensional topography of corticopontine projections from rat sensorimotor cortex: Comparisons with corticostriatal projections reveal diverse integrative organization

Journal of Comparative Neurology

Volumn 478, Issue 3, 2004, Pages 306-322

  Leergaard, Trygve B ^a   Alloway, Kevin D ^b   Pham, Tuyet A T ^a   Bolstad, Ingeborg ^a   Hoffer, Zachary S ^b   Pettersen, Christian ^a   Bjaalie, Jan G ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

3 D reconstruction; Basal ganglia; Cerebellum; Motor cortex; Pontine nuclei; Somatosensory cortex

Indexed keywords

TRACER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN CORTEX; BRAIN MAPPING; CEREBELLUM; CORTICOPONTINE TRACT; CORTICOSTRIATAL PROJECTION; MALE; NEOSTRIATUM; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORIMOTOR CORTEX; THREE DIMENSIONAL IMAGING; TOPOGRAPHY; VIBRISSA;

ANIMALS; BIOTIN; BRAIN MAPPING; DEXTRANS; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; HISTOCYTOCHEMISTRY; IMAGING, THREE-DIMENSIONAL; MALE; MOTOR CORTEX; NEOSTRIATUM; NEURAL PATHWAYS; PONS; RATS; RATS, SPRAGUE-DAWLEY; RHODAMINES; SOMATOSENSORY CORTEX;

EID: 4744373452     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20289     Document Type: Article

References (97)

1. Aldridge JW, Berridge KC. 1998. Coding of serial order by neostriatal neurons: a "natural action" approach to movement sequence. J Neurosci 18:2777-2787.
2. Alexander GE, Crutcher MD. 1990. Neural representations of the target (goal) of visually guided arm movements in three motor areas of the monkey. J Neurophysiol 64:164-178.
3. Alexander GE, DeLong MR, Strick PL. 1986. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357-381.
4. Alexander GE, Crutcher MD, DeLong MR. 1990. Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. Prog Brain Res 85:119-146.
5. Allen GI, Tsukahara N. 1974. Cerebrocerebellar communication systems. Physiol Rev 54:957-1006.
6. Alloway KD, Mutic JJ, Hoover JE. 1998. Divergent corticostriatal projections from a single cortical column in the somatosensory cortex of rats. Brain Res 785:341-346.
7. Alloway KD, Crist J, Mutic JJ, Roy SA. 1999. Corticostriatal projections from rat barrel cortex have an anisotropic organization that correlates with vibrissal whisking behavior. J Neurosci 19:10908-10922.
8. Alloway KD, Mutic JJ, Hoffer ZS, Hoover JE. 2000. Overlapping corticostriatal projections from the rodent vibrissal representations in primary and secondary somatosensory cortex. J Comp Neurol 426:51-67.
9. Alloway KD, Hoffer ZS, Hoover JE. 2003. Quantitative comparisons of corticothalamic topography within the ventrobasal complex and the posterior nucleus of the rodent thalamus. Brain Res 968:54-68.
10. Bajo VM, Merchán MA, Malmierca MS, Nodal FR, Bjaalie JG. 1999. Topographic organization of the dorsal nucleus of the lateral lemniscus in the cat. J Comp Neurol 407:349-366.
11. Berg BG, Almaas TJ, Bjaalie JG, Mustaparta H. 1998. The macroglomerular complex of the antennal lobe in the tobacco budworm moth Heliothis virescens: specified subdivision in four compartments according to information about biologically significant compounds. J Comp Physiol A 183:669-682.
12. Bjaalie JG, Brodal P. 1989. Visual pathways to the cerebellum: segregation in the pontine nuclei of terminal fields from different visual cortical areas in the cat. Neuroscience 29:95-107.
13. Bjaalie JG, Leergaard TB. 2000. Functions of the pontine nuclei in cerebrocerebellar communication. Trends Neurosci 23:152-153.
14. Bjaalie JG, Daehlen M., Stensby TV. 1997a. Surface modelling from biomedical data. In: Daehlen M, Tveito A, editors. Numerical methods and software tools in industrial mathematics. Boston: Birkhauser. p 9-26.
15. Bjaalie JG, Sudbo J, Brodal P. 1997b. Corticopontine terminal fibres form small scale clusters and large scale lamellae in the cat. Neuroreport 8:1651-1655.
16. Bower JM. 1997. Control of sensory data acquisition. Int Rev Neurobiol 41:489-513.
17. Brevik A, Leergaard TB, Svanevik M, Bjaalie JG. 2001. Three-dimensional computerised atlas of the rat brain stem precerebellar system: approaches for mapping, visualization, and comparison of spatial distribution data. Anat Embryol (Berl) 204:319-332.
18. Brodal P. 1968. The corticopontine projection in the cat. I. Demonstration of a somatotopically organized projection from the primary sensorimotor cortex. Exp Brain Res 5:210-234.
19. Brodal P. 1978. Principles of organization of the monkey corticopontine projection. Brain Res 148:214-218.
20. Brodal A. 1981. Neurological anatomy in relation to clinical medicine. Oxford: Oxford University Press.
21. Brodal P. 1983. Principles of organization of the corticopontocerebellar projection to crus II in the cat with particular reference to the parietal cortical areas. Neuroscience 10:621-638.
22. Brodal P. 1987. Organization of cerebropontocerebellar connections as studied with anterograde and retrograde transport of HRP-WGA in the cat. In: King JS, editor. New concepts in cerebellar neurobiology. New York: Alan R. Liss, Inc. p 151-182.
23. Brodal P, Bjaalie JG. 1992. Organization of the pontine nuclei. Neurosci Res 13:83-118.
24. Brodal P, Bjaalie JG. 1997. Salient anatomic features of the corticopontocerebellar pathway. Prog Brain Res 114:227-249.
25. Brodal P, Bjaalie JG, Aas JE. 1991. Organization of cingulo- pontocerebellar connections in the cat. Anat Embryol (Berl) 184:245-254.
26. Brown LL, Schneider JS, Lidsky TI. 1997. Sensory and cognitive functions of the basal ganglia. Curr Opin Neurobiol 7:157-163.
27. Brown LL, Smith DM, Goldbloom LM. 1998. Organizing principles of cortical integration in the rat neostriatum: corticostriate map of the body surface is an ordered lattice of curved laminae and radial points. J Comp Neurol 392:468-488.
28. Chapin JK, Lin CS. 1984. Mapping the body representation in the SI cortex of anesthetized and awake rats. J Comp Neurol 229:199-213.
29. Cromwell HC, Berridge KC. 1996. Implementation of action sequences by a neostriatal site: a lesion mapping study of grooming syntax. J Neurosci 16:3444-3458.
30. Donoghue JP, Wise SP. 1982. The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J Comp Neurol 212:76-88.
31. Fabri M, Burton H. 1991. Ipsilateral cortical connections of primary somatic sensory cortex in rats. J Comp Neurol 311:405-424.
32. Flaherty AW, Graybiel AM. 1991. Corticostriatal transformations in the primate somatosensory system. Projections from physiologically mapped body-part representations. J Neurophysiol 66:1249-1263.
33. Flaherty AW, Graybiel AM. 1993. Two input systems for body representations in the primate striatal matrix: experimental evidence in the squirrel monkey. J Neurosci 13:1120-1137.
34. Flaherty AW, Graybiel AM. 1995. Motor and somatosensory corticostriatal projection magnifications in the squirrel monkey. J Neurophysiol 74:2638-2648.
35. Gao JH, Parsons LM, Bower JM, Xiong J, Li J, Fox PT. 1996. Cerebellum implicated in sensory acquisition and discrimination rather than motor control. Science 272:545-547.
36. Glickstein M, May JG III, Mercier BE. 1985. Corticopontine projection in the macaque: the distribution of labeled cortical cells after large injections of horseradish peroxidase in the pontine nuclei. J Comp Neurol 235:343-359.
37. Goldman-Rakic PS, Selemon LD. 1990. New frontiers in basal ganglia research. Trends Neurosci 13:241-244.
38. Graybiel AM, Kimura M. 1995. Adaptive neural networks in the basal ganglia. In: Houk JC, Davis JL, Beiser DG, editors. Models of information processing in the basal ganglia. Cambridge, MA: MIT Press. p 103-116.
39. Hall RD, Lindholm EP. 1974. Organization of motor and somatosensory neocortex in the albino rat. Brain Res 66:23-38.
40. Hartmann-von Monakow K, Akert K, Künzle H. 1981. Projection of precentral, premotor and prefrontal cortex to the basilar pontine grey and to nucleus reticularis tegmenti pontis in the monkey (Macaca fascicularis). Arch Suisses Neurol Neurochir Psychiat 129:189-208.
41. Heimer L, Zahm DS, Alheid GF. 1995. Basal ganglia. In: Paxinos G, editor. The rat nervous system. San Diego: Academic Press, Inc. p 579-628.
42. He SQ, Dum RP, Strick PL. 1993. Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere. J Neurosci 13:952-980.
43. Hoffer ZS, Alloway KD. 2001. Organization of corticostriatal projections from the vibrissal representations in the primary motor and somatosensory cortical areas of rodents. J Comp Neurol 439:87-103.
44. Hoffer ZS, Hoover JE, Alloway KD. 2003. Sensorimotor corticocortical projections from rat barrel cortex have an anisotropic organization that facilitates integration of inputs from whiskers in the same row. J Comp Neurol 466:525-544.
45. Hoover JE, Strick PL. 1993. Multiple output channels in the basal ganglia. Science 259:819-821.
46. Hoover JE, Hoffer ZS, Alloway KD. 2003. Projections from primary somatosensory cortex to the neostriatum: the role of somatotopic continuity in corticostriatal convergence. J Neurophysiol 89:1576-1587.
47. Inase M, Sakai ST, Tanji J. 1996. Overlapping corticostriatal projections from the supplementary motor area and the primary motor cortex in the macaque monkey: an anterograde double labeling study. J Comp Neurol 373:283-296.
48. Künzle H. 1975. Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study in Macaca fascicularis. Brain Res 88:195-209.
49. Künzle H. 1977. Projections from the primary somatosensory cortex to basal ganglia and thalamus in the monkey. Exp Brain Res 30:481-492.
50. Lanciego JL, Wouterlood FG. 1994. Dual anterograde axonal tracing with Phaseolus vulgaris-leucoagglutinin (PHA-L) and biotinylated dextran amine (BDA). Neurosci Protocols 94-050-06-01-13.
51. Leergaard TB. 2003. Clustered and laminar topographic patterns in rat cerebro-pontine pathways. Anat Embryol (Berl) 206:149-162.
52. Leergaard TB, Bjaalie JG. 1995. Semi-automatic data acquisition for quantitative neuroanatomy. MicroTrace-computer programme for recording of the spatial distribution of neuronal populations. Neurosci Res 22:231-243.
53. Leergaard TB, Lakke EA, Bjaalie JG. 1995. Topographical organization in the early postnatal corticopontine projection: a carbocyanine dye and 3-D computer reconstruction study in the rat. J Comp Neurol 361:77-94.
54. Leergaard TB, Alloway KD, Mutic JJ, Bjaalie JG. 2000a. Three-dimensional topography of corticopontine projections from rat barrel cortex: correlations with corticostriatal organization. J Neurosci 20:8474-8484.
55. Leergaard TB, Lyngstad KA, Thompson JH, Taeymans S, Vos BP, De Schutter E, Bower JM, Bjaalie JG. 2000b. Rat somatosensory cerebropontocerebellar pathways: spatial relationships of the somatotopic map of the primary somatosensory cortex are preserved in a three-dimensional clustered pontine map. J Comp Neurol 422:246-266.
56. Legg CR, Mercier B, Glickstein M. 1989. Corticopontine projection in the rat: the distribution of labeled cortical cells after large injections of horseradish peroxidase in the pontine nuclei. J Comp Neurol 286:427-441.
57. Lillehaug S, Oyan D, Leergaard TB, Bjaalie JG. 2002. Comparison of semi-automatic and automatic data acquisition methods for studying three-dimensional distributions of large neuronal populations and axonal plexuses. Network 13:343-356.
58. Malach R. 1994. Cortical columns as devices for maximizing neuronal diversity. Trends Neurosci 17:101-104.
59. Malmierca MS, Leergaard TB, Bajo VM, Bjaalie JG, Merchán MA. 1998. Anatomic evidence of a three-dimensional mosaic pattern of tonotopic organization in the ventral complex of the lateral lemniscus in Cat. J Neurosci 18:10603-10618.
60. Merchán MA, Saldaña E, Plaza I. 1994. Dorsal nucleus of the lateral lemniscus in the rat: concentric organization and tonotopic projection to the inferior colliculus. J Comp Neurol 342:259-278.
61. Mercier BE, Legg CR, Glickstein M. 1990. Basal ganglia and cerebellum receive different somatosensory information in rats. Proc Natl Acad Sci U S A 87:4388-4392.
62. Middleton FA, Strick PL. 2000. Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Rev 31:236-250.
63. Mihailoff GA, McArdle CB, Adams CE. 1981. The cytoarchitecture, cytology, and synaptic organization of the basilar pontine nuclei in the rat. I. Nissl and Golgi studies. J Comp Neurol 195:181-201.
64. Mihailoff GA, Lee H, Watt CB, Yates R. 1985. Projections to the basilar pontine nuclei from face sensory and motor regions of the cerebral cortex in the rat. J Comp Neurol 237:251-263.
65. Mizuno N, Mochizuki K, Akimoto C, Matsushima R, Sasaki K. 1973. Projections from the parietal cortex to the brain stem nuclei in the cat, with special reference to the parietal cerebro-cerebellar system. J Comp Neurol 147:511-522.
66. Nambu A. 2004. A new dynamic model of the cortico-basal ganglia loop. Prog Brain Res 143:461-466.
67. Nambu A, Kaneda K, Tokuno H, Takada M. 2002. Organization of corticostriatal motor inputs in monkey putamen. J Neurophysiol 88:1830-1842.
68. Neafsey EJ, Bold EL, Haas G, Hurley-Gius KM, Quirk G, Sievert CF, Terreberry RR. 1986. The organization of the rat motor cortex: a microstimulation mapping study. Brain Res 396:77-96.
69. Oka H, Sasaki K, Matsuda Y, Yasuda T, Mizuno N. 1975. Responses of pontocerebellar neurons to stimulation of the parietal association and the frontal motor cortices. Brain Res 93:399-407.
70. Parent A, Hazrati LN. 1995. Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Rev 20:91-127.
71. Parsons LM, Fox PT. 1997. Sensory and cognitive functions. Int Rev Neurobiol 41:255-271.
72. Parsons LM, Bower JM, Gao JH, Xiong J, Li J, Fox PT. 1997. Lateral cerebellar hemispheres actively support sensory acquisition and discrimination rather than motor control. Learn Mem 4:49-62.
73. Parthasarathy HB, Schall JD, Graybiel AM. 1992. Distributed but convergent ordering of corticostriatal projections: analysis of the frontal eye field and the supplementary eye field in the macaque monkey. J Neurosci 12:4468-4488.
74. Potter RF, Rüegg DG, Wiesendanger M. 1978. Responses of neurons of the pontine nuclei to stimulation of the sensorimotor, visual and auditory cortex of rats. Brain Res Bull 3:15-19.
75. Ramanathan S, Hanley JJ, Deniau JM, Bolam JP. 2002. Synaptic convergence of motor and somatosensory cortical afferents onto GABAergic interneurons in the rat striatum. J Neurosci 22:8158-8169.
76. Reiner A, Veenman CL, Medina L, Jiao Y, Del Mar N, Honig MG. 2000. Pathway tracing using biotinylated dextran amines. J Neurosci Methods 103:23-37.
77. Rosenquist AC. 1985. Connections of visual cortical areas in the cat. In: Peters A, Jones EG, editors. Cerebral cortex. New York: Plenum Press. p 81-117.
78. Rüegg DG, Wiesendanger M. 1975. Corticofugal effects from sensorimotor area I and somatosensory area II on neurones of the pontine nuclei in the cat. J Physiol 247:745-757.
79. Rüegg DG, Sequin JJ, Wiesendanger M. 1977. Effects of electrical stimulation of somatosensory and motor areas of the cerebral cortex on neurons of the pontine nuclei in squirrel monkeys. Neuroscience 2:923-927.
80. Ruigrok TJH, Cella F. 1995. Precerebellar nuclei and red nucleus. In: Paxinos G, editor. The rat nervous system. San Diego: Academic Press, Inc. p 277-308.
81. Schmahmann JD. 1997. Rediscovery of an early concept. Int Rev Neurobiol 41:3-27.
82. Schmahmann JD. 1998. Dysmetria of thought: clinical consequences of cerebellar dysfunction on cognition and affect. Trends Cogn Sci 2:362-371.
83. Schmahmann JD, Pandya DN. 1997. The cerebrocerebellar system. Int Rev Neurobiol 41:31-60.
84. Schwarz C, Möck M. 2001. Spatial arrangement of cerebro-pontine terminals. J Comp Neurol 435:418-432.
85. Schwarz C, Thier P. 1995. Modular organization of the pontine nuclei: dendritic fields of identified pontine projection neurons in the rat respect the borders of cortical afferent fields. J Neurosci 15:3475-3489.
86. Schwarz C, Thier P. 1999. Binding of signals relevant for action: towards a hypothesis of the functional role of the pontine nuclei. Trends Neurosci 22:443-451.
87. Selemon LD, Goldman-Rakic PS. 1990. Topographic intermingling of striatonigral and striatopallidal neurons in the rhesus monkey. J Comp Neurol 297:359-376.
88. Takakusaki K, Oohinata-Sugimoto J, Saitoh K, Habaguchi T. 2004. Role of basal ganglia-brainstem systems in the control of postural muscle tone and locomotion. Prog Brain Res 143:231-237.
89. Torigoe Y, Blanks RH, Precht W. 1986. Anatomical studies on the nucleus reticularis tegmenti pontis in the pigmented rat. II. Subcortical afferents demonstrated by the retrograde transport of horseradish peroxidase. J Comp Neurol 243:88-105.
90. Vassbo K, Nicotra G, Wiberg M, Bjaalie JG. 1999. Monkey somatosensory cerebrocerebellar pathways: uneven densities of corticopontine neurons in different body representations of areas 3b, 1, and 2. J Comp Neurol 406:109-128.
91. Welker WI. 1964. Analysis of the sniffing behavior of the albino rat. Behavior 22:223-244.
92. Welker C. 1971. Microelectrode delineation of fine grain somatotopic organization of (SmI) cerebral neocortex in albino rat. Brain Res 26:259-275.
93. Welker C. 1976. Receptive fields of barrels in the somatosensory neocortex of the rat. J Comp Neurol 166:173-189.
94. Wiesendanger R, Wiesendanger M. 1982a. The corticopontine system in the rat. I. Mapping of corticopontine neurons. J Comp Neurol 208:215-226.
95. Wiesendanger R, Wiesendanger M. 1982b. The corticopontine system in the rat. II. The projection pattern. J Comp Neurol 208:227-238.
96. Wiesendanger R, Wiesendanger M, Rüegg DG. 1979. An anatomical investigation of the corticopontine projection in the primate (Macaca fascicularis and Saimiri sciureus) - II. The projection from frontal and parental association areas. Neuroscience 4:747-765.
97. Wong-Riley M. 1979. Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res 171:11-28.