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. 1996 Aug 6;93(16):8683–8687. doi: 10.1073/pnas.93.16.8683

The temporal lobe is a target of output from the basal ganglia.

F A Middleton 1, P L Strick 1
PMCID: PMC38733  PMID: 8710931

Abstract

The basal ganglia are known to receive inputs from widespread regions of the cerebral cortex, such as the frontal, parietal, and temporal lobes. Of these cortical areas, only the frontal lobe is thought to be the target of basal ganglia output. One of the cortical regions that is a source of input to the basal ganglia is area TE, in inferotemporal cortex. This cortical area is thought to be critically involved in the recognition and discrimination of visual objects. Using retrograde transneuronal transport of herpes simplex virus type 1, we have found that one of the output nuclei of the basal ganglia, the substantia nigra pars reticulata, projects via the thalamus to TE. Thus, TE is not only a source of input to the basal ganglia, but also is a target of basal ganglia output. This result implies that the output of the basal ganglia influences higher order aspects of visual processing. In addition, we propose that dysfunction of the basal ganglia loop with TE leads to alterations in visual perception, including visual hallucinations.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albin R. L., Young A. B., Penney J. B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989 Oct;12(10):366–375. doi: 10.1016/0166-2236(89)90074-x. [DOI] [PubMed] [Google Scholar]
  2. Baizer J. S., Desimone R., Ungerleider L. G. Comparison of subcortical connections of inferior temporal and posterior parietal cortex in monkeys. Vis Neurosci. 1993 Jan-Feb;10(1):59–72. doi: 10.1017/s0952523800003229. [DOI] [PubMed] [Google Scholar]
  3. Brysch W., Brysch I., Creutzfeldt O. D., Schlingensiepen R., Schlingensiepen K. H. The topology of the thalamo-cortical projections in the marmoset monkey (Callithrix jacchus). Exp Brain Res. 1990;81(1):1–17. doi: 10.1007/BF00230095. [DOI] [PubMed] [Google Scholar]
  4. Buerger A. A., Gross C. G., Rocha-Miranda C. E. Effects of ventral putamen lesions on discrimination learning by monkeys. J Comp Physiol Psychol. 1974 Mar;86(3):440–446. doi: 10.1037/h0036142. [DOI] [PubMed] [Google Scholar]
  5. Cummings J. L. Behavioral complications of drug treatment of Parkinson's disease. J Am Geriatr Soc. 1991 Jul;39(7):708–716. doi: 10.1111/j.1532-5415.1991.tb03627.x. [DOI] [PubMed] [Google Scholar]
  6. DeLong M. R. Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 1990 Jul;13(7):281–285. doi: 10.1016/0166-2236(90)90110-v. [DOI] [PubMed] [Google Scholar]
  7. Divac I., Lavail J. H., Rakic P., Winston K. R. Heterogeneous afferents to the inferior parietal lobule of the rhesus monkey revealed by the retrograde transport method. Brain Res. 1977 Mar 11;123(2):197–207. doi: 10.1016/0006-8993(77)90474-7. [DOI] [PubMed] [Google Scholar]
  8. Divac I., Rosvold H. E., Szwarcbart M. K. Behavioral effects of selective ablation of the caudate nucleus. J Comp Physiol Psychol. 1967 Apr;63(2):184–190. doi: 10.1037/h0024348. [DOI] [PubMed] [Google Scholar]
  9. Dunn D. W., Weisberg L. A., Nadell J. Peduncular hallucinations caused by brainstem compression. Neurology. 1983 Oct;33(10):1360–1361. doi: 10.1212/wnl.33.10.1360. [DOI] [PubMed] [Google Scholar]
  10. Factor S. A., Molho E. S., Podskalny G. D., Brown D. Parkinson's disease: drug-induced psychiatric states. Adv Neurol. 1995;65:115–138. [PubMed] [Google Scholar]
  11. François C., Yelnik J., Percheron G., Fénelon G. Topographic distribution of the axonal endings from the sensorimotor and associative striatum in the macaque pallidum and substantia nigra. Exp Brain Res. 1994;102(2):305–318. doi: 10.1007/BF00227517. [DOI] [PubMed] [Google Scholar]
  12. Grofova I., Deniau J. M., Kitai S. T. Morphology of the substantia nigra pars reticulata projection neurons intracellularly labeled with HRP. J Comp Neurol. 1982 Jul 10;208(4):352–368. doi: 10.1002/cne.902080406. [DOI] [PubMed] [Google Scholar]
  13. Herkenham M. The afferent and efferent connections of the ventromedial thalamic nucleus in the rat. J Comp Neurol. 1979 Feb 1;183(3):487–517. doi: 10.1002/cne.901830304. [DOI] [PubMed] [Google Scholar]
  14. Hikosaka O., Wurtz R. H. Visual and oculomotor functions of monkey substantia nigra pars reticulata. I. Relation of visual and auditory responses to saccades. J Neurophysiol. 1983 May;49(5):1230–1253. doi: 10.1152/jn.1983.49.5.1230. [DOI] [PubMed] [Google Scholar]
  15. Hoover J. E., Strick P. L. Multiple output channels in the basal ganglia. Science. 1993 Feb 5;259(5096):819–821. doi: 10.1126/science.7679223. [DOI] [PubMed] [Google Scholar]
  16. Ilinsky I. A., Jouandet M. L., Goldman-Rakic P. S. Organization of the nigrothalamocortical system in the rhesus monkey. J Comp Neurol. 1985 Jun 15;236(3):315–330. doi: 10.1002/cne.902360304. [DOI] [PubMed] [Google Scholar]
  17. Jacobs D. H., Shuren J., Heilman K. M. Impaired perception of facial identity and facial affect in Huntington's disease. Neurology. 1995 Jun;45(6):1217–1218. doi: 10.1212/wnl.45.6.1217. [DOI] [PubMed] [Google Scholar]
  18. Kasdon D. L., Jacobson S. The thalamic afferents to the inferior parietal lobule of the rhesus monkey. J Comp Neurol. 1978 Feb 15;177(4):685–706. doi: 10.1002/cne.901770409. [DOI] [PubMed] [Google Scholar]
  19. Kemp J. M., Powell T. P. The connexions of the striatum and globus pallidus: synthesis and speculation. Philos Trans R Soc Lond B Biol Sci. 1971 Sep 30;262(845):441–457. doi: 10.1098/rstb.1971.0106. [DOI] [PubMed] [Google Scholar]
  20. Levinson D. F. Pharmacologic treatment of schizophrenia. Clin Ther. 1991 May-Jun;13(3):326–352. [PubMed] [Google Scholar]
  21. Lynch J. C., Hoover J. E., Strick P. L. Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport. Exp Brain Res. 1994;100(1):181–186. doi: 10.1007/BF00227293. [DOI] [PubMed] [Google Scholar]
  22. Markowitsch H. J., Emmans D., Irle E., Streicher M., Preilowski B. Cortical and subcortical afferent connections of the primate's temporal pole: a study of rhesus monkeys, squirrel monkeys, and marmosets. J Comp Neurol. 1985 Dec 15;242(3):425–458. doi: 10.1002/cne.902420310. [DOI] [PubMed] [Google Scholar]
  23. McKee A. C., Levine D. N., Kowall N. W., Richardson E. P., Jr Peduncular hallucinosis associated with isolated infarction of the substantia nigra pars reticulata. Ann Neurol. 1990 May;27(5):500–504. doi: 10.1002/ana.410270508. [DOI] [PubMed] [Google Scholar]
  24. Middleton F. A., Strick P. L. Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. Science. 1994 Oct 21;266(5184):458–461. doi: 10.1126/science.7939688. [DOI] [PubMed] [Google Scholar]
  25. Minciacchi D., Bentivoglio M., Molinari M., Kultas-Ilinsky K., Ilinsky I. A., Macchi G. Multiple cortical targets of one thalamic nucleus: the projections of the ventral medial nucleus in the cat studied with retrograde tracers. J Comp Neurol. 1986 Oct 1;252(1):106–129. doi: 10.1002/cne.902520107. [DOI] [PubMed] [Google Scholar]
  26. Mishkin M. A memory system in the monkey. Philos Trans R Soc Lond B Biol Sci. 1982 Jun 25;298(1089):83–95. doi: 10.1098/rstb.1982.0074. [DOI] [PubMed] [Google Scholar]
  27. Miyashita Y. Inferior temporal cortex: where visual perception meets memory. Annu Rev Neurosci. 1993;16:245–263. doi: 10.1146/annurev.ne.16.030193.001333. [DOI] [PubMed] [Google Scholar]
  28. PENFIELD W., PEROT P. THE BRAIN'S RECORD OF AUDITORY AND VISUAL EXPERIENCE. A FINAL SUMMARY AND DISCUSSION. Brain. 1963 Dec;86:595–696. doi: 10.1093/brain/86.4.595. [DOI] [PubMed] [Google Scholar]
  29. Parent A., Bouchard C., Smith Y. The striatopallidal and striatonigral projections: two distinct fiber systems in primate. Brain Res. 1984 Jun 15;303(2):385–390. doi: 10.1016/0006-8993(84)91224-1. [DOI] [PubMed] [Google Scholar]
  30. Saint-Cyr J. A., Ungerleider L. G., Desimone R. Organization of visual cortical inputs to the striatum and subsequent outputs to the pallido-nigral complex in the monkey. J Comp Neurol. 1990 Aug 8;298(2):129–156. doi: 10.1002/cne.902980202. [DOI] [PubMed] [Google Scholar]
  31. Schmahmann J. D., Pandya D. N. Anatomical investigation of projections from thalamus to posterior parietal cortex in the rhesus monkey: a WGA-HRP and fluorescent tracer study. J Comp Neurol. 1990 May 8;295(2):299–326. doi: 10.1002/cne.902950212. [DOI] [PubMed] [Google Scholar]
  32. Silbersweig D. A., Stern E., Frith C., Cahill C., Holmes A., Grootoonk S., Seaward J., McKenna P., Chua S. E., Schnorr L. A functional neuroanatomy of hallucinations in schizophrenia. Nature. 1995 Nov 9;378(6553):176–179. doi: 10.1038/378176a0. [DOI] [PubMed] [Google Scholar]
  33. Smith Y., Hazrati L. N., Parent A. Efferent projections of the subthalamic nucleus in the squirrel monkey as studied by the PHA-L anterograde tracing method. J Comp Neurol. 1990 Apr 8;294(2):306–323. doi: 10.1002/cne.902940213. [DOI] [PubMed] [Google Scholar]
  34. Tanaka K., Saito H., Fukada Y., Moriya M. Coding visual images of objects in the inferotemporal cortex of the macaque monkey. J Neurophysiol. 1991 Jul;66(1):170–189. doi: 10.1152/jn.1991.66.1.170. [DOI] [PubMed] [Google Scholar]
  35. Tigges J., Tigges M., Cross N. A., McBride R. L., Letbetter W. D., Anschel S. Subcortical structures projecting to visual cortical areas in squirrel monkey. J Comp Neurol. 1982 Jul 20;209(1):29–40. doi: 10.1002/cne.902090104. [DOI] [PubMed] [Google Scholar]
  36. Tigges J., Walker L. C., Tigges M. Subcortical projections to the occipital and parietal lobes of the chimpanzee brain. J Comp Neurol. 1983 Oct 10;220(1):106–115. doi: 10.1002/cne.902200110. [DOI] [PubMed] [Google Scholar]
  37. Vonsattel J. P., Myers R. H., Stevens T. J., Ferrante R. J., Bird E. D., Richardson E. P., Jr Neuropathological classification of Huntington's disease. J Neuropathol Exp Neurol. 1985 Nov;44(6):559–577. doi: 10.1097/00005072-198511000-00003. [DOI] [PubMed] [Google Scholar]
  38. Webster M. J., Bachevalier J., Ungerleider L. G. Subcortical connections of inferior temporal areas TE and TEO in macaque monkeys. J Comp Neurol. 1993 Sep 1;335(1):73–91. doi: 10.1002/cne.903350106. [DOI] [PubMed] [Google Scholar]
  39. Yeterian E. H., Pandya D. N. Corticostriatal connections of extrastriate visual areas in rhesus monkeys. J Comp Neurol. 1995 Feb 13;352(3):436–457. doi: 10.1002/cne.903520309. [DOI] [PubMed] [Google Scholar]
  40. Zemanick M. C., Strick P. L., Dix R. D. Direction of transneuronal transport of herpes simplex virus 1 in the primate motor system is strain-dependent. Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):8048–8051. doi: 10.1073/pnas.88.18.8048. [DOI] [PMC free article] [PubMed] [Google Scholar]

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