Experimental Brain Research

, Volume 98, Issue 3, pp 523–534 | Cite as

Inter-subject variability of cerebral activations in acquiring a motor skill: a study with positron emission tomography

  • Gottfried Schlaug
  • Uwe Knorr
  • Rüdiger J. Seitz
Original Paper


Cerebral structures activated during sequential right-hand finger movements were mapped with regional cerebral blood flow (rCBF) measurements by positron emission tomography (PET) in individual subjects. Nine healthy volunteers were examined twice; after initial learning and after practicing the finger movement sequence for more than 1 h. Task-specific activation sites were identified by statistical distributions of maximal activity and region size in rCBF subtraction images. A consistent task specific activation in all nine subjects was detected in the contralateral sensorimotor cortex at an average movement rate of 3.2 Hz reached after practice. This corresponded to a significant increase of the mean rCBF in the left primary sensorimotor cortex in spatially standardised and averaged PET images. Additional task specific activation sites detected by individual analysis were found in the lateral and medial premotor, parietal, and cingulate areas, and in subcortical structures including the basal ganglia of both cerebral hemispheres. These activations showed no or little spatial overlap from subject to subject, thus being obscured in the analysis of pooled data. The observed activity patterns were related to movement rate and accuracy in individual subjects. It is suggested that the rCBF changes associated with acquisition of a motor skill in individual humans may correspond to plasticity of sensorimotor representations reported in monkeys.

Key words

positron emission tomography Regional cerebral blood flow Motor learning Brain mapping Human 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alexander GE (1987) Selective neuronal discharge in monkey putamen reflects intended direction of planned limb movements. Exp Brain Res 67:623–634Google Scholar
  2. Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Ann Rev Neurosci 9:357–381Google Scholar
  3. Baleydier C, Mauguiere F (1980) The duality of the cingulate gyrus in monkey. Brain 103:525–554Google Scholar
  4. Bergström M, Boethius J, Eriksson L, Greitz T, Widen L (1981) Head fixation device for reproducible position alignement in transmission CT and positron emission tomography. J Comput Assist Tomogr 5:136–141Google Scholar
  5. Braak H (1976) A primitive gigantopyramidal field buried in the depth of the cingulate sulcus of the human brain. Brain Res 109:219–233Google Scholar
  6. Brooks VB (1990) Limbic assistance in task related use of motor skill. In: Eccles JC, Creutzfeldt O (eds) The principle of design and operation of the brain. Springer, Berlin Heidelberg New York, pp 343–368Google Scholar
  7. Brooks VB, Hilperath F, Ross H-G, Brooks M, Freund H-J (1992) Strategy selection triggers movement scaling. Soc Neurosci Abstr 18:647.10Google Scholar
  8. Brotchie P, Iansek R, Horne MK (1991) Motor function of the monkey globus pallidus. I. Neuronal discharge and parameters of movement. II. Cognitive aspects of movement and phasic neuronal activity. Brain 114:1667–1702Google Scholar
  9. Canavan AGM, Nixon PD, Passingham RE (1989) Motor learning in monkeys (Macaca fascicularis) with lesions in motor thalamus. Exp Brain Res 77:113–126Google Scholar
  10. Cavada C, Goldman-Rakic PS (1989) Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections, II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. J Comp Neurol 287:393–445PubMedGoogle Scholar
  11. Chollet F, DiPiero V, Wise RJS, Brooks DJ, Dolan RJ, Frackowiak RSJ (1991) The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann Neurol 29:64–71Google Scholar
  12. Crutcher MD, DeLong MR (1984) Single cell studies of the primate putamen. I. Functional Organization, II. Relation of direction of movement and pattern of muscular activity. Exp Brain Res 53:233–258Google Scholar
  13. Deecke L (1987) Bereitschaftpotential as an indicator of movement preparation in supplementary motor area and motor cortex. In: Porter R (ed) Motor areas of the cerebral cortex. Wiley, Chichester, pp 231–245Google Scholar
  14. Deiber MP, Passingham RE, Colebatch JG, Friston KJ, Nixon PD, Frackowiak RSJ (1991) Cortical areas and the selection of movement: a study with positron emission tomography. Exp Brain Res 84:393–402PubMedGoogle Scholar
  15. DeLong MR (1972) Activity of basal ganglia neurons during movement. Brain Res 40:127–135Google Scholar
  16. Dum RP, Strick PL (1991) The origin of corticospinal projections from the premotor areas in the frontal lobe. J Neurosci 11:667–689PubMedGoogle Scholar
  17. Eichenbaum H, Otto T, Cohen NJ (1992) Review. The hipocampus what does it do? Behav Neural Biol 57:2–36Google Scholar
  18. Eidelberg D, Galaburda AM (1984) Inferior parietal lobule. Arch Neurol 41:843–852Google Scholar
  19. Evans AC, Beil C, Marrett S, Thompson CJ, Hakim A (1988) Anatomical-functional correlation using an adjustable MRI based region of interest atlas with positron emission tomography. J Cereb Blood Flow Metab 8:513–530Google Scholar
  20. Fiez JA, Petersen SE, Cheney MK, Raichle ME (1992) Impaired nonmotor learning and error detection associated with cerebellar damage. Brain 115:155–178Google Scholar
  21. Filimonoff IN (1932) Über die Variabilität der Großhirnrindenstruktur. II Regio occipitalis beim erwachsenen Menschen. J Psychol Neurol 44:1–96Google Scholar
  22. Fox PT, Raichle ME (1984) Stimulus rate dependence of regional cerebral blood flow in human striate cortex, demonstrated by positron emission tomography. J Neurophysiol 51:1109–1120Google Scholar
  23. Fox PT, Perlmutter JS, Raichle ME (1985) A stereotactic method of anatomical localization for positron emission tomography. J Comput Assist Tomogr 9:141–153Google Scholar
  24. Fox PT, Pardo JV, Petersen SE, Raichle ME (1987) Supplementary motor and premotor responses to actual and imagined hand movements with positron emission tomography. Soc Neurosci Abstr 13:398.10Google Scholar
  25. Fox PT, Mintun MA, Reiman EM, Raichle ME (1988) Enhanced detection of focal brain responses using intersubject averaging and change distribution analysis of subtracted PET images. J Cereb Blood Flow Metab 8:642–653Google Scholar
  26. Friston KJ, Fith CD, Liddle PF, Frakowiak RSJ (1991a) Comparing functional (PET) images: the assessment of significant change. J Cereb Blood Flow Metab 11:690–699Google Scholar
  27. Friston KJ, Frith CD, Liddle PF, Frackowiak RSJ (1991b) The cerebellum in skill learning. J Cereb Blood Flow Metab 11 [Suppl2]:S440Google Scholar
  28. Galyon DD, Strick PL (1985) Multiple and differential projections from the parietal lobe to the premotor areas of the primate. Soc Neurosci Abstr 11:373.10Google Scholar
  29. Goldman-Rakic PS, Porrino LJ (1985) The primate mediodorsal nucleus and its projection to the frontal lobe. J Comp Neurol 242:535–560Google Scholar
  30. Grafton ST, Woods RP, Mazziotta JC, Phelps ME (1991) Somatotopic mapping of the primary motor cortex in humans: activation studies with cerebral blood flow and positron emission tomography. J Neurophysiol 66:735–743Google Scholar
  31. Greitz T, Bohm C, Holte S, Eriksson L (1991) A computerised brain atlas: construction, anatomical content, and some applications. J Comput Ass Tomogr 15:26–38Google Scholar
  32. Halsband U, Freund HJ (1990) Premotor cortex and conditional motor learning in man. Brain 113:207–222Google Scholar
  33. Hutchins KD, Martina AM, Strick PL (1988) Corticospinal projections from the medial wall of the hemisphere. Exp Brain Res 71:667–672PubMedGoogle Scholar
  34. Ilinsky IA, Kultas-Ilinsky K (1987) Sagittal cytoarchitectonic maps of the Macaco, mulatto thalamus with a revised nomenclature of the motorrelated nuclei validated by observations on their connectivity. J Comp Neurol 262:331–364Google Scholar
  35. Inhoff AW, Diener HC, Rafal RD, Ivry R (1989) The role of cerebellar structures in the execution of serial movements. Brain 112:565–581Google Scholar
  36. Jenkins IH, Passinghman RE, Nixon PD, Frackowiak RSJ Brooks DJ (1992) The learning of motor sequences: a PET study.Eur J Neurosci S:3077Google Scholar
  37. Kemp JM and Powell TPS (1970) The cortico-striate projection in the monkey. Brain 93:525–546Google Scholar
  38. Kihlstrom JF (1987) The cognition unconscious. Science 237:1445–1457Google Scholar
  39. Knorr U, Weder B, Kleinschmidt A, Wirrwar A, Huang Y, Herzog H, Seitz RJ (1993) Identification of task specific rCBF changes in individual subjects: validation and application for PET. J Comput Assist Tomogr 17:517–528Google Scholar
  40. 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 88:195–209Google Scholar
  41. Litton J, Bergström M, Eriksson L, Bohm C, Blomqvist G, Kesselberg M (1984) Performance study of the PC-384 positron camera system for emission tomography of the brain. J Comput Assist Tomogr 8:74–87Google Scholar
  42. Luppino G, Matelli M, Rizzolatti G (1990) Corticocortical connections of two electrophysiologically identified arm representations in the mesial agranular frontal cortex. Exp Brain Res 82:214–218PubMedGoogle Scholar
  43. Luppino G, Matelli M, Camarda RM, Gallese V, Rizzolatti G (1991) Multiple representations of body movements in mesial area 6 and the adjacent cingulate cortex: an intracortical microstimulation study in the macaque monkey. J Comp Neurol 311:463–482PubMedGoogle Scholar
  44. Matelli MG, Luppino G, Rizzolatti G (1991) Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey. J Comp Neurol 311:445–462PubMedGoogle Scholar
  45. Matelli M, Luppino G, Camarda R, Rizzolatti G (1992) Thalmic input to area F3 (SMA-Proper) and to area F6 (Pre-SMA) in the macaque monke. Soc Neuroscience AbstrlS:214.10Google Scholar
  46. Mazziotta JC, Phelps ME, Wapenski J (1985) Human cerebral motor system metabolic responses in health and disease. J Cereb Blood Flow Metab 5 [Suppl 1]:S213-S214Google Scholar
  47. Milliken GW, Nudo RJ, Grenda R, Jenkins WM, Merzenich MM (1992) Expansion of distal forelimb representation in primary motor cortex of adult squirrel monkeys following motor training. Soc Neurosci Abstr 22:214.13Google Scholar
  48. Morecraft HJ, Van Hoesen GW (1988) Somatotopical organization of the cingulate projections to the primary and supplementary motor cortices in the old world monkey. Soc Neurosci Abstr 14:329.5Google Scholar
  49. Muakkassa KF, Strick PL (1979) Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized ‘premotor’ areas. Brain Res 177:176–182Google Scholar
  50. Mushiake H, Inase M, Tanji J (1990) Selective coding of motor sequence in the supplementary motor area of the monkey cerebral cortex. Exp Brain Res 82:208–210Google Scholar
  51. Nudo RJ, Jenkins WM, Merzenich MM, Prejean T, Grenda R (1992) Neurophysiological correlates of hand preference in primary motor cortex of adult squirrel monkeys. J Neurosci 12:2918–2947Google Scholar
  52. Okano K, Tanji J (1987) Neuronal activity in the primate motor fields of the agranular frontal cortex preceding visually triggered and self paced movements. Exp Brain Res 66:155–166Google Scholar
  53. Olesen J (1974) Cerebral blood blow methods for measurement regulation effects of drugs and changes in disease. Fadls Forlag, Copenhagen, Århus, OdenseGoogle Scholar
  54. Pardo JV, Pardo PJ, Janer KW, Raichle ME (1990) The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm. Proc Natl Acad Sci USA 87:256–259Google Scholar
  55. Petrides M, Pandya DN (1984) Projections to the frontal lobes from the posterior parietal region in the rhesus monkey. J Comp Neurol 228:105–116PubMedGoogle Scholar
  56. Raichle ME (1987) Circulatory and metabolic correlates of brain function in normal humans. In: Plum F (ed) Handbook of physiology, sect 1, The nervous system, vol V. American Physiological Society, Bethesda, Md, pp 643–674Google Scholar
  57. Recanzone GH, Merzenich MM, Jenkins WM, Grajski KA, Dinse HR (1992a) Topographic reorganization of the hand representation in cortical area 3b of owl monkeys trained in a frequency discrimination task. J Neurophysiol 67:1031–1056Google Scholar
  58. Recanzone GH, Merzenich MM, Jenkins WM (1992b) Frequency discrimination training engaging restricted skin surface results in an emergence of a cutaneous response zone in cortical area 3a. J Neurophysiol 67:1057–1070Google Scholar
  59. Roland PE, Larsen B, Lassen NA, Skinhoj E (1980a) Supplementary motor area and other cortical areas in organizing of voluntary movements in man. J Neurophysiol. 43:118–136Google Scholar
  60. Roland PE, Skinhoj E, Lassen NA, Larsen B (1980b) Different cortical areas in man in organization of voluntary movement in extrapersonal space. J Neurophysiol 43:137–150Google Scholar
  61. Roland PE, Meyer E, Yamamoto YL, Thompson CJ (1982) Regional cerebral blood flow changes in cortex and basal ganglia during voluntary movements in normal human volunteers. J Neurophysiol 48:467–480Google Scholar
  62. Roland PE, Eriksson L, Stone-Elander S, Widen L (1987) Does mental activity change the oxidative metabolism of the brain? J Neurosci 7:2373–2389Google Scholar
  63. Roland PE, Eriksson L, Widen L, Stone-Elander S (1989) Changes in regional cerebral oxidative metabolism induced by tactile learning and recognition in man. Eur J Neurosci 1:3–18Google Scholar
  64. Schieber MH (1990) How might the motor cortex individuate movements? Trends Neurosci 13:440–445Google Scholar
  65. Schieber MH (1992) Widely distributed neuron activity in primary motor cortex hand area during individuated finger movements. Soc Neurosci Abstr 18:214.1Google Scholar
  66. Schlaug G, Knorr U, Seitz RJ (1992a) Size and peak values are determinants for cerebral activation areas in neurobehavioral studies with positron emission tomography. Eur J Neurosci 5:S2321Google Scholar
  67. Schlaug G, Knorr U, Seitz RJ (1992b) Inter-subject variability of cerebral activation in motor learning. Soc Neurosci Abstr 22:361.12Google Scholar
  68. Schultz W, Romo R (1988) Neuronal activity in the monkey striaturn during the initiation of movements. Exp Brain Res 71:431–436Google Scholar
  69. Seal J, Gross C, Bioulac B (1982) Activity of neurons in area 5 during a simple arm movement in monkeys before and after deafferentation of the trained limb. Brain Res 250:229–243Google Scholar
  70. Seitz RJ, Roland PE (1992a) Learning of sequential finger movements in man: a combined kinematic and positron emission tomography (PET) study. Eur J Neurosci 4:154–165Google Scholar
  71. Seitz RJ, Roland PE (1992b) Variability of the regional cerebral blood flow pattern studied with [11C]-fluoromethane and positron emission tomography (PET). Comp Med Imaging Graphics 16:311–322Google Scholar
  72. Seitz RJ, Bohm C, Greitz T, Roland PE, Eriksson E, Blomqvist G, Rosenqvist G, Nordeil B (1990a) Accuracy and precision of the computerized brain atlas programme for localization and quantification in positron emission tomography. J Cereb Blood Flow Metab 10:443–457Google Scholar
  73. Seitz RJ, Roland PE, Bohm C, Greitz T, Eriksson L, StoneElander S (1990b) Motor learning in man: a positron emission tomographic study. Neuroreport 1:57–66Google Scholar
  74. Seitz RJ, Herzog H, Steinmetz H, Roden W, Benecke R, Freund H-J (1991) Motor activity after subcortical stroke studied with positron emission tomography (PET). J Cereb Blood Flow Metab 11 [Suppl 2]:S647Google Scholar
  75. Seitz RJ, Knorr U, Schlaug G, Weder B (1993) Comparison of inter-subject averaging and individual response identification for mapping of motor function in the human brain with positron emission tomography. Ann Nucl Med 7 [Suppl]: S114-S115Google Scholar
  76. Shima K, Aya K, Mushiake H, Inase M, Aizawa H, Tanji J (1991) Two movement related foci in the primate cingulate cortex observed in signal-triggered and self paced forelimb movements. J Neurophysiol 65:188–202PubMedGoogle Scholar
  77. Squire LR (1986) Mechanisms of memory. Science 232:1612–1619Google Scholar
  78. Steinmetz H, Seitz RJ (1991) Functional anatomy of language processing: neuroimaging and the problem of individual variability. Neuropsychologia 29:1149–1161Google Scholar
  79. Steinmetz H, Huang Y, Seitz RJ, Knorr U, Schlaug G, Herzog H, Hackländer T, Freund HJ (1992) Individual integration of positron emission tomography and highresolution magnetic resonance imaging. J Cereb Blood Flow Metab 12:919–926Google Scholar
  80. Stensaas SS, Eddington DK, Dobelle WH (1974) The topography and variability of the primary visual cortex in man. J Neurosurg 40:747–755PubMedGoogle Scholar
  81. Talairach J, Tournoux P (1988) Coplanar stereotaxic atlas of the human brain. 3-dimensional proportional system: an approach to cerebral imaging. Thieme, Stuttgart New YorkGoogle Scholar
  82. Tanji J, Tanaguchi K, Saga T (1980) The supplementary motor area: neuronal responses to motor instructions. J Neurophysiol 43:60–68Google Scholar
  83. Thach WT, Goodkin HP, Keating JG (1992) The cerebellum and the adaptive coordination of movement. Ann Rev Neurosci 15:403–442CrossRefPubMedGoogle Scholar
  84. Thompson RF (1986) The neurobiology of learning and memory. Science 233:941–947Google Scholar
  85. Vogt BA, Pandya DN (1987) Cingulate cortex in rhesus monkey. II. Cortical afferents. J Comp Neurol 262:271–289Google Scholar
  86. Vogt BA, Finch DM, Oison CR (1992) Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. Cerebral Cortex 2:435–443Google Scholar
  87. Walter H, Kristeva R, Knorr U, Schlaug G, Huang Y, Steinmetz H, Nebeling B, Herzog H, Seitz RJ (1992) Individual somatotopy of primary sensorimotor cortex revealed by intermodal matching of MEG, PET, and MRI. Brain Topogr 5:183–187Google Scholar
  88. Watson IDG, Shipp S, Frackowiak RSJ, Zeki S (1992) Area V5 of human visual cortex identified in individuals using PET and magnetic resonance imaging. Soc Neurosci Abstr 22:585.5Google Scholar
  89. 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 (in press)Google Scholar
  90. Weiller C, Chollet F, Friston KJ, Wise RJS, Frackowiak RSJ (1992a) Functional reorganization of the brain in recovery from striatocapsular infarction in man. Ann Neurol 31:463–472Google Scholar
  91. Weiller C, Friston KJ, Frackowiak RSJ (1992b) Examples of functional reorganisation of the human cerebral cortex after capsular infarcts a PET activation study. J Neurology 239:832Google Scholar
  92. Weinrich M, Wise SP (1982) The premotor cortex of the monkey. J Neurosci 2:1329–1345PubMedGoogle Scholar
  93. Weinrich M, Wise SP, Mauritz KH (1984) A neurophysiological study of premotor cortex in the rhesus monkey. Brain 107:385–414PubMedGoogle Scholar
  94. Wise SP (1985) The primate premotor cortex: Past, present, and preparatory. Ann Rev Neurosci 8:1–19Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • Gottfried Schlaug
    • 1
  • Uwe Knorr
    • 1
  • Rüdiger J. Seitz
    • 1
  1. 1.Department of NeurologyHeinrich-Heine-UniversityGermany

Personalised recommendations