Abstract
There are two great subcortical circuits that relay sensory information to motor structures in the mammalian brain. One pathway relays via the pontine nuclei and cerebellum, and the other relays by way of the basal ganglia. We studied the cells of origin of these two major pathways from the posteromedial barrel subfield of rats, a distinct region of the somatosensory cortex that contains the sensory representation of the large whiskers. We injected tracer substances into the caudate putamen or the pontine nuclei and charted the location of retrogradely filled cortical cells. In preliminary studies, we used double-labeling techniques to determine whether the cells of origin of these two pathways send axon collaterals to other subcortical targets. Lamina V of the rat posteromedial barrel subfield contains two distinct populations of subcortically projecting neurons, which are organized into distinct sublamina. . Corticopontine cells are located exclusively in sublamina Vb, the deeper of two sublamina revealed by cytochrome oxidase staining. Corticostriate cells are located almost exclusively in the more superficial sublamina Va. Experiments using double-labeling fluorescent tracers demonstrate that about one-quarter of the corticopontine cells send a collateral branch to the superior colliculus. Other studies have shown that cells in Vb are activated at very short latency after vibrissal stimulation; hence, they would seem to be an appropriate relay for the rapid transmission of sensory information to the cerebellum for use in sensory guidance of movement.
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- Blake D. J., Zarzecki P., Somjen G. G. Electrophysiological study of corticocaudate projections in cats. J Neurobiol. 1976 Mar;7(2):143–156. doi: 10.1002/neu.480070207. [DOI] [PubMed] [Google Scholar]
- Brodal P., Dietrichs E., Bjaalie J. G., Nordby T., Walberg F. Is lectin-coupled horseradish peroxidase taken up and transported by undamaged as well as by damaged fibers in the central nervous system? Brain Res. 1983 Nov 14;278(1-2):1–9. doi: 10.1016/0006-8993(83)90221-4. [DOI] [PubMed] [Google Scholar]
- Catsman-Berrevoets C. E., Kuypers H. G. A search for corticospinal collaterals to thalamus and mesencephalon by means of multiple retrograde fluorescent tracers in cat and rat. Brain Res. 1981 Aug 10;218(1-2):15–33. doi: 10.1016/0006-8993(81)90986-0. [DOI] [PubMed] [Google Scholar]
- Donoghue J. P., Herkenham M. Neostriatal projections from individual cortical fields conform to histochemically distinct striatal compartments in the rat. Brain Res. 1986 Feb 19;365(2):397–403. doi: 10.1016/0006-8993(86)91658-6. [DOI] [PubMed] [Google Scholar]
- Donoghue J. P., Kitai S. T. A collateral pathway to the neostriatum from corticofugal neurons of the rat sensory-motor cortex: an intracellular HRP study. J Comp Neurol. 1981 Sep 1;201(1):1–13. doi: 10.1002/cne.902010102. [DOI] [PubMed] [Google Scholar]
- Endo K., Araki T., Yagi N. The distribution and pattern of axon branching of pyramidal tract cells. Brain Res. 1973 Jul 27;57(2):484–491. doi: 10.1016/0006-8993(73)90154-6. [DOI] [PubMed] [Google Scholar]
- Gibson A. R., Hansma D. I., Houk J. C., Robinson F. R. A sensitive low artifact TMB procedure for the demonstration of WGA-HRP in the CNS. Brain Res. 1984 Apr 30;298(2):235–241. doi: 10.1016/0006-8993(84)91423-9. [DOI] [PubMed] [Google Scholar]
- Gibson A., Baker J., Mower G., Glickstein M. Corticopontine cells in area 18 of the cat. J Neurophysiol. 1978 Mar;41(2):484–495. doi: 10.1152/jn.1978.41.2.484. [DOI] [PubMed] [Google Scholar]
- Ivy G. O., Gould H. J., 3rd, Killackey H. P. Variability in the distribution of callosal projection neurons in the adult rat parietal cortex. Brain Res. 1984 Jul 23;306(1-2):53–61. doi: 10.1016/0006-8993(84)90355-x. [DOI] [PubMed] [Google Scholar]
- Jinnai K., Matsuda Y. Neurons of the motor cortex projecting commonly on the caudate nucleus and the lower brain stem in the cat. Neurosci Lett. 1979 Jul;13(2):121–126. doi: 10.1016/0304-3940(79)90028-4. [DOI] [PubMed] [Google Scholar]
- Jones E. G., Coulter J. D., Burton H., Porter R. Cells of origin and terminal distribution of corticostriatal fibers arising in the sensory-motor cortex of monkeys. J Comp Neurol. 1977 May 1;173(1):53–80. doi: 10.1002/cne.901730105. [DOI] [PubMed] [Google Scholar]
- Kassel J. Somatotopic organization of SI corticotectal projections in rats. Brain Res. 1982 Jan 14;231(2):247–255. doi: 10.1016/0006-8993(82)90363-8. [DOI] [PubMed] [Google Scholar]
- Kawamura S., Diamond I. T. The laminar origin of descending projections from the cortex to the thalamus in Tupaia glis. Brain Res. 1978 Sep 22;153(2):333–339. doi: 10.1016/0006-8993(78)90411-0. [DOI] [PubMed] [Google Scholar]
- Keizer K., Kuypers H. G., Huisman A. M., Dann O. Diamidino yellow dihydrochloride (DY . 2HCl); a new fluorescent retrograde neuronal tracer, which migrates only very slowly out of the cell. Exp Brain Res. 1983;51(2):179–191. doi: 10.1007/BF00237193. [DOI] [PubMed] [Google Scholar]
- Keller A., White E. L., Cipolloni P. B. The identification of thalamocortical axon terminals in barrels of mouse Sml cortex using immunohistochemistry of anterogradely transported lectin (Phaseolus vulgaris-leucoagglutinin). Brain Res. 1985 Sep 16;343(1):159–165. doi: 10.1016/0006-8993(85)91171-0. [DOI] [PubMed] [Google Scholar]
- Killackey H. P., Belford G. R. The formation of afferent patterns in the somatosensory cortex of the neonatal rat. J Comp Neurol. 1979 Jan 15;183(2):285–303. doi: 10.1002/cne.901830206. [DOI] [PubMed] [Google Scholar]
- Kitai S. T., Kocsis J. D., Wood J. Origin and characteristics of the cortico-caudate afferents: an anatomical and electrophysiological study. Brain Res. 1976 Dec 10;118(1):137–141. doi: 10.1016/0006-8993(76)90848-9. [DOI] [PubMed] [Google Scholar]
- Land P. W., Simons D. J. Cytochrome oxidase staining in the rat SmI barrel cortex. J Comp Neurol. 1985 Aug 8;238(2):225–235. doi: 10.1002/cne.902380209. [DOI] [PubMed] [Google Scholar]
- Legg C. R., Mercier B., Glickstein M. Corticopontine projection in the rat: the distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei. J Comp Neurol. 1989 Aug 22;286(4):427–441. doi: 10.1002/cne.902860403. [DOI] [PubMed] [Google Scholar]
- Mihailoff G. A., Burne R. A., Woodward D. J. Projections of the sensorimotor cortex to the basilar pontine nuclei in the rat: an autoradiographic study. Brain Res. 1978 Apr 28;145(2):347–354. doi: 10.1016/0006-8993(78)90867-3. [DOI] [PubMed] [Google Scholar]
- Mihailoff G. A., Watt C. B., Burne R. A. Evidence suggesting that both the corticopontine and cerebellopontine systems are each composed of two separate neuronal populations: an electron microscopic and horseradish peroxidase study in the rat. J Comp Neurol. 1981 Jan 10;195(2):221–242. doi: 10.1002/cne.901950204. [DOI] [PubMed] [Google Scholar]
- Miller R. Distribution and properties of commissural and other neurons in cat sensorimotor cortex. J Comp Neurol. 1975 Dec 1;164(3):361–373. doi: 10.1002/cne.901640307. [DOI] [PubMed] [Google Scholar]
- Oka H., Jinnai K. Common projection of the motor cortex to the caudate nucleus and the cerebellum. Exp Brain Res. 1978 Jan 18;31(1):31–42. doi: 10.1007/BF00235802. [DOI] [PubMed] [Google Scholar]
- Roger M., Cadusseau J. Afferent connections of the nucleus posterior thalami in the rat, with some evolutionary and functional considerations. J Hirnforsch. 1984;25(5):473–485. [PubMed] [Google Scholar]
- Royce G. J. Laminar origin of cortical neurons which project upon the caudate nucleus: a horseradish peroxidase investigation in the cat. J Comp Neurol. 1982 Feb 10;205(1):8–29. doi: 10.1002/cne.902050103. [DOI] [PubMed] [Google Scholar]
- Schwab M., Agid Y., Glowinski J., Thoenen H. Retrograde axonal transport of 125I-tetanus toxin as a tool for tracing fiber connections in the central nervous system; connections of the rostral part of the rat neostriatum. Brain Res. 1977 May 6;126(2):211–224. doi: 10.1016/0006-8993(77)90722-3. [DOI] [PubMed] [Google Scholar]
- Strick P. L. How do the basal ganglia and cerebellum gain access to the cortical motor areas? Behav Brain Res. 1985 Nov-Dec;18(2):107–123. doi: 10.1016/0166-4328(85)90067-1. [DOI] [PubMed] [Google Scholar]
- Veening J. G., Cornelissen F. M., Lieven P. A. The topical organization of the afferents to the caudatoputamen of the rat. A horseradish peroxidase study. Neuroscience. 1980;5(7):1253–1268. doi: 10.1016/0306-4522(80)90198-0. [DOI] [PubMed] [Google Scholar]
- Wiesendanger R., Wiesendanger M. The corticopontine system in the rat. I. Mapping of corticopontine neurons. J Comp Neurol. 1982 Jul 1;208(3):215–226. doi: 10.1002/cne.902080302. [DOI] [PubMed] [Google Scholar]
- Wiesendanger R., Wiesendanger M. The corticopontine system in the rat. II. The projection pattern. J Comp Neurol. 1982 Jul 1;208(3):227–238. doi: 10.1002/cne.902080303. [DOI] [PubMed] [Google Scholar]
- Wilson C. J. Morphology and synaptic connections of crossed corticostriatal neurons in the rat. J Comp Neurol. 1987 Sep 22;263(4):567–580. doi: 10.1002/cne.902630408. [DOI] [PubMed] [Google Scholar]
- Wise S. P., Jones E. G. Cells of origin and terminal distribution of descending projections of the rat somatic sensory cortex. J Comp Neurol. 1977 Sep 15;175(2):129–157. doi: 10.1002/cne.901750202. [DOI] [PubMed] [Google Scholar]
- Wise S. P., Jones E. G. Somatotopic and columnar organization in the corticotectal projection of the rat somatic sensory cortex. Brain Res. 1977 Sep 16;133(2):223–235. doi: 10.1016/0006-8993(77)90760-0. [DOI] [PubMed] [Google Scholar]
- Wise S. P., Murray E. A., Coulter J. D. Somatotopic organization of corticospinal and corticotrigeminal neurons in the rat. Neuroscience. 1979;4(1):65–78. doi: 10.1016/0306-4522(79)90218-5. [DOI] [PubMed] [Google Scholar]
- Wong-Riley M. T. Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci. 1989 Mar;12(3):94–101. doi: 10.1016/0166-2236(89)90165-3. [DOI] [PubMed] [Google Scholar]
- Wong-Riley M. Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res. 1979 Jul 27;171(1):11–28. doi: 10.1016/0006-8993(79)90728-5. [DOI] [PubMed] [Google Scholar]
- Woolsey T. A., Van der Loos H. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res. 1970 Jan 20;17(2):205–242. doi: 10.1016/0006-8993(70)90079-x. [DOI] [PubMed] [Google Scholar]