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Impaired somatosensory discrimination of shape in Parkinson's disease: Association with caudate nucleus dopaminergic function

Bruno J Weder 1,✉, Klaus L Leenders 2,3, Peter Vontobel 2, Matthias Nienhusmeier 1, Alex Keel 4, Wolfgang Zaunbauer 5, Thomas Vonesch 1, Hans‐Peter Ludin 1
PMCID: PMC6873336  PMID: 10432178

Abstract

Tactile discrimination of macrogeometric objects in a two‐alternative forced‐choice procedure represents a demanding task involving somatosensory pathways and higher cognitive processing. The objects for somatosensory discrimination, i.e., rectangular parallelepipeds differing only in oblongness, were presented in sequential pairs to normal volunteers and 12 parkinsonian patients. The performance of patients was significantly impaired compared to normal volunteers. From a biochemical point of view, the patients were characterized by a severely reduced 6‐[18F]‐fluoro‐L‐dopa (FDOPA) tracer metabolism in the basal ganglia, as measured using positron emission tomography (PET). Furthermore, reduced specific FDOPA metabolism in the putamen was consistent with the impaired motor capacities of the patients. The reduced specific FDOPA‐uptake within the caudate nucleus was associated with additionally diminished somatosensory discrimination. This association, of low perception during task performance and decreased FDOPA‐uptake, provides direct evidence for the role of the caudate nucleus in the cognitive part of the task. We suggest that directed attention and working memory were critically involved as a result of disturbed interactions between the head of the caudate nucleus and the dorsolateral prefrontal cortex. Furthermore, there were indications of an additional involvement of the mesolimbic system, which might be of importance during challenging situations such as forced choice. We conclude that differential effects on parts of the basal ganglia, during evolution of the degenerative process characteristic of Parkinson's disease, have profound consequences on the performance of skills, as shown here for a somatosensory discrimination task. Hum. Brain Mapping 8:1–12, 1999. © 1999 Wiley‐Liss, Inc.

Keywords: macrogeometric objects, somatosensory discrimination, Parkinson's disease, 6‐[18F]‐fluoro‐L‐dopa, dorsolateral prefrontal circuit, directed attention, working memory

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REFERENCES

  1. Agid Y, Javoy‐Agid F, Ruberg M. 1987. Biochemistry of neurotransmitters in Parkinson's disease: an overview In: Marsden CD, Fahn S, editors. Movement disorders 2. London: Butterworth; p 166–230. [Google Scholar]
  2. Alexander GE, DeLong MR, Strick PL. 1986. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357–381. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=86213671&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  3. Antonini A, Vontobel P, Psylla M, Günther I, Maguire PR, Missimer J, Leenders KL. 1995. Complementary positron emission tomographic studies of the striatal dopaminergic system in Parkinson's disease. Arch Neurol 52:1183–1190. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=96094929&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  4. Benecke R, Rothwell JC, Dick JPR, Day BL, Marsden CD. 1987. Performance of simultaneous motor movements in patients with Parkinson's disease. Brain 109:361–379. [DOI] [PubMed] [Google Scholar]
  5. Berns GS, Cohen JD, Mintun MA. 1997. Brain region responsive to novelty in the absence of awareness. Science 276:1272–1275. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=97301862&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  6. Caplan LR, Schmahmann JD, Kase CS, Feldmann E, Baquis G, Greenberg JP, Gorelick PB, Helgason C, Hier DB. 1990. Caudate infarcts. Arch Neurol 47:133–143. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=90147130&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  7. Corbetta M, Miezin FM, Dobmeyer S, Shulman GL, Petersen SE. 1990. Attentional modulation of neural processing of shape, color, and velocity in humans. Science 248:1556–1559. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=90296083&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  8. Dawson‐Saunders B, Trapp RG. 1990. Basic and clinical biostatistics. London: Prentice‐Hall. [Google Scholar]
  9. Divac I, Rosvold HE, Szwarcbart MK. 1967. Behavioral effects of selective ablation of the caudate nucleus. J Comp Physiol Psychol 63:184–190. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=68004062&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  10. Dolan RJ, Fletcher P, Frith CD, Friston KJ, Frackowiack RSJ, Grasby PM. 1995. Dopaminergic modulation of impaired cognitive activation in the anterior cingulate cortex in schizophrenia. Nature 378:180–182. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=96069734&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  11. Doyon J, Owen AM, Dagher A, Chertkow H, Evans AC. 1998. Abnormal basal ganglia outflow in Parkinson's disease associated with motor sequence learning. Neuroimage 7:996. [Google Scholar]
  12. Fletcher PC, Frith CD, Rugg MD. 1997. The functional neuroanatomy of episodic memory. Trends Neurosci 20:213–218. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=97285989&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  13. Freund H‐J. 1987. Abnormalities of motor behavior after cortical lesions in humans. Handbook of physiology—“the nervous system V. Bethesda: American Physiological Society; p 763–810. [Google Scholar]
  14. Fuster JM. 1981. Prefrontal cortex in motor control In: Brookhart JM, Mountcastle VB, Brooks VB, editors. Handbook of physiology, section 1, the nervous system, volume 2, motor control, part 2 Bethesda: American Physiological Society; p 1017–1061. [Google Scholar]
  15. Fuster JM, Alexander GE. 1973. Firing changes in cells of the nucleus medialis dorsalis associated with delayed response behavior. Brain Res 61:79–91. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=74083833&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  16. Gibson JJ. 1962. Observations on active touch. Psychol Rev 69:477–491. [DOI] [PubMed] [Google Scholar]
  17. Goldman PS, Rosvold HE, Vest B, Galkin TW. 1971. Analysis of the delayed‐alternation deficit produced by dorsolateral prefrontal lesions in the rhesus monkey. J Comp Physiol Psychol 77:212–220. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=72033822&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  18. Goldman‐Rakic PS. 1989. Cortical localization of working memory In: McGaugh JL, Weinberger NM, Lynch G, editors. Brain organization and memory: cells, systems and circuits. New York: Oxford University Press; p 1–29. [Google Scholar]
  19. Greitz T, Bohm C, Holte S, Eriksson L. 1990. A computerized brain atlas: construction, anatomical content, and some applications. J Comput Assist Tomogr 15:26–38. [PubMed] [Google Scholar]
  20. Hazeltine E, Grafton ST, Ivry R. 1997. Attention and stimulus characteristics determine the locus of motor‐sequence encoding. A PET study. Brain 120:123–140. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=97208861&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  21. Hornykiewicz O. 1981. Brain neurotransmitter changes in Parkinson's disease In: Marsden CD, Fahn S, editors. Movement disorders. London: Butterworth; p 427–442. [Google Scholar]
  22. Isseroff A, Rosvold HE, Galkin TW, Goldman‐Rakic PS. 1982. Spatial memory impairments following damage to the mediodorsal nucleus of the thalamus in rhesus monkeys. Brain Res 232:97–113. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=82114611&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  23. Ledermann SJ, Klatzky RL. 1987. Hand movements: a window into haptic object recognition. Cogn Psychol 19:342–368. [DOI] [PubMed] [Google Scholar]
  24. Leenders KL, Wolfson L, Gibbs JM, Wise RJS, Causon R, Jones T, Legg N. 1985. The effect of L‐dopa on regional cerebral blood flow and oxygen metabolism in patients with Parkinson's disease. Brain 108:171–181. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=85150982&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  25. Leenders KL, Salmon EP, Tyrrel P, Perani D, Brooks DJ, Sager H, Jones T, Marsden CD, Frackowiak RSJ. 1990. The nigrostriatal dopaminergic system assessed in vivo by positron emission tomography in healthy volunteers and patients with Parkinson's disease. Arch Neurol 47:1290–1297. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=91069305&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  26. Loranger AW, Goodell H, McDowell FH, Lee JE, Sweet RD. 1972. Intellectual impairment in Parkinson's disease. Brain 106:257–270. [DOI] [PubMed] [Google Scholar]
  27. Martínez‐Martín P, Gil‐Nagel A, Morlán Gracia L, Balseiro Gómez J, Martínez‐Sarriés J, Bermejo F, Cooperative Multicentric Group . 1994. Unified Parkinson's disease rating scale characteristics and structure. Mov Dis 9:76–83. [DOI] [PubMed] [Google Scholar]
  28. Mesulam MM. 1990. Large‐scale neurocognitive networks and distributed processing for attention, language, and memory. Ann Neurol 28:597–613. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=91083309&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  29. Nahmias C, Garnett ES, Firnau G, Lang A. 1985. Striatal dopamine distribution in parkinsonian patients during life. J Neurol Sci 69:223–230. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=85291908&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  30. Oldfield RC. 1971. The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9:97–113. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=72164093&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  31. Owen AM, Doyon J, Petrides M, Evans AC. 1996. Planning and spatial working memory: a positron emission tomography study in humans. Eur J Neurosci 8:353–364. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=96325518&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  32. Pardo JV, Fox PT, Raichle ME. 1991. Localization of a human system for sustained attention by positron emission tomography. Nature 349:61–64. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=91087918&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  33. Parent A, Hazrati L‐N. 1995. Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res Rev 20:128–154. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=95227208&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  34. Patlak CS, Blasberg RG. 1985. Graphical evaluation of blood‐to‐brain transfer constants from multiple‐time uptake data: generalizations. J Cereb Blood Flow Metab 5:584–590. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=86034229&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  35. Paus T, Petrides M, Evans AC, Meyer E. 1993. Role of the anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. J Neurophysiol 70:453–469. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=94015258&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  36. Pirozzolo FJ, Hansch EC, Mortimer JA, Webster DD, Kuskowski MA. 1982. Dementia in Parkinson's disease: a neuropsychological analysis. Brain Cogn 1:71–83. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=86215671&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  37. Playford ED, Jenkins IH, Passingham RE, Nutt J, Frackowiak RSJ, Brooks DJ. 1992. Impaired mesial frontal and putamen activation in Parkinson's disease: a positron emission tomography study. Ann Neurol 32:151–161. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=92378132&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  38. Quinn NP, Husain FA. 1986. Parkinson's disease. Br Med J [Clin Res] 293:379–382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Roland PE. 1987. Somatosensory detection of microgeometry, macrogeometry and kinesthesia after localized lesions of the cerebral hemispheres in man. Brain Res Rev 12:43–94. [DOI] [PubMed] [Google Scholar]
  40. Roland PE. 1993. Brain activation. New York: Wiley‐Liss; p 83–86. [Google Scholar]
  41. Roland PE, Mortensen E. 1987. Somatosensory detection of microgeometry, macrogeometry and kinesthesia in man. Brain Res Rev 12:1–42. [DOI] [PubMed] [Google Scholar]
  42. Ruff HA. 1984. Infants' manipulative exploration of objects: effects of age and object characteristics. Dev Psychol 20:9–20. [Google Scholar]
  43. Sawaguchi T, Matsumara M, Kubota K. 1990a. Catecholaminergic effects on neuronal activity related to a delayed response task in monkey prefrontal cortex. J Neurophysiol 63:1385–1400. [DOI] [PubMed] [Google Scholar]
  44. Sawaguchi T, Matsumara M, Kubota K. 1990b. Effects of dopamine antagonists on neuronal activity related to a delayed response task in monkey prefrontal cortex. J Neurophysiol 63:1401–1412. [DOI] [PubMed] [Google Scholar]
  45. Scatton B, Javoy‐Agid F, Rouquier L, Dubois B, Agid Y. 1983. Reduction of cortical dopamine, noradrenaline, serotonine, and their metabolites in Parkinson's disease. Brain Res 275:321–328. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=84025594&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  46. Seitz RJ, Roland PE. 1992. Learning of sequential finger movements in man: a combined kinematic and positron emission tomography (PET) study. Eur J Neurosci 4:154–165. [DOI] [PubMed] [Google Scholar]
  47. Seitz RJ, Roland PE, Bohm C, Greitz T, Stone‐Elander S. 1991. Somatosensory discrimination of shape: tactile exploration and cerebral activation. Eur J Neurosci 3:481–492. [DOI] [PubMed] [Google Scholar]
  48. Stam CJ, Visser SL, Op de Coul AAW, De Sonneville LMJ, Schellens RLLA, Brunia CHM, de Smet JS, Gielen G. 1993. Disturbed frontal regulation of attention in Parkinson's disease. Brain 116:1139–1158. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=94036076&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  49. Steriade M, McCarley RW. 1990. Brain stem control of wakefulness and sleep. New York: Plenum Press; p 125. [Google Scholar]
  50. Thurfjell L, Bohm C, Bengtsson E. 1995. CBA —“an atlas based software tool used to facilitate the interpretation of neuroimaging data. Comput Methods Programs Biomed 47:51–71. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=96053900&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  51. Wall PD. 1970. The sensory and motor role of impulses travelling in the dorsal columns towards cerebral cortex. Brain 93:505–524. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=71003161&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  52. Weder B, Seitz RJ. 1994. Deficient cerebral activation pattern in stroke recovery. Neuroreport 5:457–460. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=94271985&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  53. Weder B, Knorr U, Herzog H, Nebeling B, Kleinschmidt A, Huang Y, Steinmetz H, Freund H‐J, Seitz RJ. 1994. Tactile exploration of shape after subcortical ischemic infarction studied with positron emission tomography. Brain 117:593–605. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=94306106&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  54. Weder B, Nienhusmeier M, Keel A, Leenders KL. 1998a. Somatosensory discrimination of shape: prediction of success in normal volunteers and parkinsonian patients. Exp Brain Res 120:104–108. [DOI] [PubMed] [Google Scholar]
  55. Weder B, Azari NP, Knorr U, Seitz RJ, Nienhusmeier M, Leenders KL, Ludin HP. 1998b. Functional brain interactions during tactile object discrimination in Parkinson's disease as compared to normals. Neuroimage 7:414. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Weingartner H, Burn S, Diebel R, Le Witt PA. 1984. Cognitive impairment in Parkinson's disease: distinguishing between effort‐demanding and automatic cognitive processes. Psychol Res 11:223–235. [DOI] [PubMed] [Google Scholar]

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