The subthalamic nucleus is one of multiple innervation sites for long-range corticofugal axons: A single-axon tracing study in the rat

Journal of Neuroscience

Volumn 32, Issue 17, 2012, Pages 5990-5999

  Kita, Takako ^a   Kita, Hitoshi ^a  

^a UNIVERSITY OF TENNESSEE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEURON SPECIFIC NUCLEAR PROTEIN; VESICULAR GLUTAMATE TRANSPORTER 2;

ANIMAL TISSUE; ARTICLE; BRAIN STEM; CEREBRAL PEDUNCLE; CORPUS STRIATUM; IMMUNOHISTOCHEMISTRY; INNERVATION; MALE; NERVE FIBER; NERVE PROJECTION; NEUROANATOMICAL TRACT TRACING; NONHUMAN; PONTINE NUCLEUS; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SPINAL CORD; SUBTHALAMIC NUCLEUS; SUPERIOR COLLICULUS; THALAMUS NUCLEUS; ZONA INCERTA;

ANIMALS; AXONS; BIOTIN; BRAIN MAPPING; CEREBRAL CORTEX; DEXTRANS; MALE; NEURAL PATHWAYS; NEURONS; PHOSPHOPYRUVATE HYDRATASE; RATS; RATS, SPRAGUE-DAWLEY; STILBAMIDINES; SUBTHALAMIC NUCLEUS; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 84860156184     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5717-11.2012     Document Type: Article

References (55)

1. Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366-375.
2. Bevan MD, Francis CM, Bolam JP (1995) The glutamate-enriched cortical and thalamic input to neurons in the subthalamic nucleus of the rat: convergence with GABA-positive terminals. J Comp Neurol 361:491-511.
3. Brecht M, Krauss A, Muhammad S, Sinai-Esfahani L, Bellanca S, Margrie TW (2004) 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.
4. Canteras NS, Shammah-Lagnado SJ, Silva BA, Ricardo JA (1990) Afferent connections of the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat. Brain Res 513:43-59.
5. Chang HT, Kuo H, Whittaker JA, Cooper NG (1990) Light and electron microscopic analysis of projection neurons retrogradely labeled with Fluoro-Gold: notes on the application of antibodies to Fluoro-Gold. J Neurosci Methods 35:31-37.
6. Cowan RL, Wilson CJ (1994) Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. J Neurophysiol 71:17-32.
7. Degos B, Deniau JM, Le Cam J, Mailly P, Maurice N (2008) Evidence for a direct subthalamo-cortical loop circuit in the rat. Eur J Neurosci 27:2599-2610.
8. DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:281-285.
9. Deschênes M, Bourassa J, Pinault D (1994) Corticothalamic projections from layer V cells in rat are collaterals of long-range corticofugal axons. Brain Res 664:215-219.
10. Donoghue JP, Kitai ST (1981) A collateral pathway to the neostriatum from corticofugal neurons of the rat sensory-motor cortex: an intracellular HRP study. J Comp Neurol 201:1-13.
11. Donoghue JP, Wise SP (1982) The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J Comp Neurol 212:76-88.
12. Donoghue JP, Kerman KL, Ebner FF (1979) Evidence for two organizational plans within the somatic sensory-motor cortex of the rat. J Comp Neurol 183:647-663.
13. Farries MA, Kita H, Wilson CJ (2010) Dynamic spike threshold and zero membrane slope conductance shape the response of subthalamic neurons to cortical input. J Neurosci 30:13180-13191.
14. Féger J, Bevan M, Crossman AR (1994) The projections from the parafascicular thalamic nucleus to the subthalamic nucleus and the striatum arise from separate neuronal populations: a comparison with the corticostriatal and corticosubthalamic efferents in a retrograde fluorescent doublelabelling study. Neuroscience 60:125-132.
15. Fujimoto K, Kita H (1993) Response characteristics of subthalamic neurons to the stimulation of the sensorimotor cortex in the rat. Brain Res 609:185-192.
16. Giuffrida R, Li Volsi G, Maugeri G, Perciavalle V (1985) Influences of pyramidal tract on the subthalamic nucleus in the cat. Neurosci Lett 54:231-235.
17. Graybiel AM, Aosaki T, Flaherty AW, Kimura M (1994) The basal ganglia and adaptive motor control. Science 265:1826-1831.
18. Grinevich V, Brecht M, Osten P (2005) Monosynaptic pathway from rat vibrissa motor cortex to facial motor neurons revealed by lentivirus-based axonal tracing. J Neurosci 25:8250-8258.
19. Hall RD, Lindholm EP (1974) Organization of motor and somatosensory neocortex of the albino rat. Brain Res 66:23-38.
20. Henderson JM, Pell M, O'Sullivan DJ, McCusker EA, Fung VS, Hedges P, Halliday GM (2002) Postmortem analysis of bilateral subthalamic electrode implants in Parkinson's disease. Mov Disord 17:133-137.
21. Hornykiewicz O (2006) The discovery of dopamine deficiency in the parkinsonian brain. J Neural Transm Suppl (70):9-15.
22. Israel Z, Bergman H (2008) Pathophysiology of the basal ganglia and movement disorders: from animal models to human clinical applications. Neurosci Biobehav Rev 32:367-377.
23. Iwahori N (1978) A Golgi study on the subthalamic nucleus of the cat. J Comp Neurol 182:383-397.
24. Kita H (1994) Physiology of two disynaptic pathways from the sensorimotor cortex to the basal ganglia output nuclei. In: The basal ganglia IV (Percheron G, McKenzie JS, Fe ́ger J, eds), pp 263-276, New York: Plenum.
25. Kita H, Chang HT, Kitai ST (1983) The morphology of intracellularly labeled rat subthalamic neurons: a light microscopic analysis. J Comp Neurol 215:245-257.
26. Kitai ST, Deniau JM (1981) Cortical inputs to the subthalamus: intracellular analysis. Brain Res 214:411-415.
27. Kitai ST, Kita H (1987) Anatomy and physiology of the subthalamic nucleus: a driving force of the basal ganglis. New York: Plenum.
28. Kolomiets BP, Deniau JM, Mailly P, Ménétrey A, Glowinski J, Thierry AM (2001) Segregation and convergence of information flow through the cortico-subthalamic pathways. J Neurosci 21:5764-5772.
29. Kubota Y, Hatada S, Kondo S, Karube F, Kawaguchi Y (2007) Neocortical inhibitory terminals innervate dendritic spines targeted by thalamocortical afferents. J Neurosci 27:1139-1150.
30. Künzle H (1978) An autoradiographic analysis of the efferent connections from premotor and adjacent prefrontal regions (areas 6 and 9) in macaca fascicularis. Brain Behav Evol 15:185-234.
31. Lehéricy S, Bardinet E, Tremblay L, Van de Moortele PF, Pochon JB, Dormont D, Kim DS, Yelnik J, Ugurbil K (2006) Motor control in basal ganglia circuits using fMRI and brain atlas approaches. Cereb Cortex 16:149-161.
32. Mediratta NK, Nicoll JA (1983) Conduction velocities of corticospinal axons in the rat studied by recording cortical antidromic responses. J Physiol 336:545-561.
33. Mitrofanis J (2005) Some certainty for the "zone of uncertainty"? Exploring the function of the zona incerta. Neuroscience 130:1-15.
34. Mitrofanis J, Mikuletic L (1999) Organisation of the cortical projection to the zona incerta of the thalamus. J Comp Neurol 412:173-185.
35. Monakow KH, Akert K, Künzle H (1979) Projections of precentral and premotor cortex to the red nucleus and other midbrain areas in Macaca fascicularis. Exp Brain Res 34:91-105.
36. Moriizumi T, Nakamura Y, Kitao Y, Kudo M (1987) Ultrastructural analyses of afferent terminals in the subthalamic nucleus of the cat with a combined degeneration and horseradish peroxidase tracing method. J Comp Neurol 265:159-174.
37. Morishima M, Morita K, Kubota Y, Kawaguchi Y (2011) Highly differentiated projection-specific cortical subnetworks. J Neurosci 31:10380-10391.
38. Murata J, Kitagawa M, Uesugi H, Saito H, Iwasaki Y, Kikuchi S, Tashiro K, Sawamura Y (2003) Electrical stimulation of the posterior subthalamic area for the treatment of intractable proximal tremor. J Neurosurg 99:708-715.
39. Nambu A, Tokuno H, Hamada I, Kita H, Imanishi M, Akazawa T, Ikeuchi Y, Hasegawa N (2000) Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus in the monkey. J Neurophysiol 84:289-300.
40. Nudo RJ, Masterton RB (1990) Descending pathways to the spinal cord, III: Sites of origin of the corticospinal tract. J Comp Neurol 296:559-583.
41. Oorschot DE (1996) Total number of neurons in the neostriatal, pallidal, subthalamic, and substantia nigral nuclei of the rat basal ganglia: a stereological study using the cavalieri and optical disector methods. J Comp Neurol 366:580-599.
42. Orieux G, François C, Féger J, Hirsch EC (2002) Consequences of dopaminergic denervation on the metabolic activity of the cortical neurons projecting to the subthalamic nucleus in the rat. J Neurosci 22:8762-8770.
43. Parent M, Parent A (2006) Single-axon tracing study of corticostriatal projections arising from primary motor cortex in primates. J Comp Neurol 496:202-213.
44. Paz JT, Deniau JM, Charpier S (2005) Rhythmic bursting in the corticosubthalamo-pallidal network during spontaneous genetically determined spike and wave discharges. J Neurosci 25:2092-2101.
45. Pearson JC, Norris JR, Phelps CH (1985) Subclassification of neurons in the subthalamic nucleus of the lesser bushbaby (Galago senegalensis): a quantitative Golgi study using principal components analysis. J Comp Neurol 238:323-339.
46. Perge JA, Niven JE, Mugnaini E, Balasubramanian V, Sterling P (2012) Why do axons differ in caliber? J Neurosci 32:626-638.
47. Périer C, Vila M, Féger J, Agid Y, Hirsch EC (2000) Functional activity of zona incerta neurons is altered after nigrostriatal denervation in hemiparkinsonian rats. Exp Neurol 162:215-224.
48. Plaha P, Ben-Shlomo Y, Patel NK, Gill SS (2006) Stimulation of the caudal zona incerta is superior to stimulation of the subthalamic nucleus in improving contralateral parkinsonism. Brain 129:1732-1747.
49. Reiner A, Jiao Y, Del Mar N, Laverghetta AV, Lei WL (2003) Differential morphology of pyramidal tract-type and intratelencephalically projecting-type corticostriatal neurons and their intrastriatal terminals in rats. J Comp Neurol 457:420-440.
50. Shammah-Lagnado SJ, Negrão N, Ricardo JA (1985) Afferent connections of the zona incerta: a horseradish peroxidase study in the rat. Neuroscience 15:109-134.
51. Tseng GF, Prince DA (1993) Heterogeneity of rat corticospinal neurons. J Comp Neurol 335:92-108.
52. Veinante P, Deschênes M (2003) Single-cell study of motor cortex projections to the barrel field in rats. J Comp Neurol 464:98-103.
53. Voges J, Volkmann J, Allert N, Lehrke R, Koulousakis A, Freund HJ, Sturm V (2002) Bilateral high-frequency stimulation in the subthalamic nucleus for the treatment of Parkinson disease: correlation of therapeutic effect with anatomical electrode position. J Neurosurg 96:269-279.
54. Wang Z, McCormick DA (1993) Control of firing mode of corticotectal and corticopontine layer V burst-generating neurons by norepinephrine, acetylcholine, and 1S,3R-ACPD. J Neurosci 13:2199-2216.
55. Yelnik J, Percheron G (1979) Subthalamic neurons in primates: a quantitative and comparative analysis. Neuroscience 4:1717-1743.