Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-23T05:06:01.409Z Has data issue: false hasContentIssue false
  • English
  • Français

Inhibitory Control of Adjacent Finger Movements while Performing a Modified Version of the Halstead Finger Tapping Test: Effects of Age, Education and Sex

Published online by Cambridge University Press:  16 November 2020

George P. Prigatano Open the ORCID record for George P. Prigatano [Opens in a new window] ,
Sandro Barbosa de Oliveira ,
Carlos Wellington Passos Goncalves ,
Sheila Marques Denucci ,
Roberta Monteiro Pereira  and
Lucia Willadino Braga
George P. Prigatano*
Affiliation:
Department of Clinical Neuropsychology, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, AZ, USA
Sandro Barbosa de Oliveira
Affiliation:
SARAH Network of Rehabilitation Hospitals, Brasilia, Brazil
Carlos Wellington Passos Goncalves
Affiliation:
SARAH Network of Rehabilitation Hospitals, Brasilia, Brazil
Sheila Marques Denucci
Affiliation:
SARAH Network of Rehabilitation Hospitals, Brasilia, Brazil
Roberta Monteiro Pereira
Affiliation:
SARAH Network of Rehabilitation Hospitals, Brasilia, Brazil
Lucia Willadino Braga
Affiliation:
SARAH Network of Rehabilitation Hospitals, Brasilia, Brazil
*
*Correspondence and reprint requests to: George P. Prigatano, Ph.D., Barrow Neurological Institute, Department of Clinical Neuropsychology, 222 West Thomas Road, Suite 315, Phoenix, AS 85013, USA. Tel: +1 602 406 3671; Fax: +1 602 406 6115. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective:

Selective motor inhibition is known to decline with age. The purpose of this study was to determine the frequency of failures at inhibitory control of adjacent finger movements while performing a repetitive finger tapping task in young, middle-aged and older adults. Potential education and sex effects were also evaluated.

Methods:

Kinematic recordings of adjacent finger movements were obtained on 107 healthy adults (ages 20–80) while they performed a modified version of the Halstead Finger Tapping Test (HTFF). Study participants were instructed to inhibit all finger movements while tapping with the index finger.

Results:

Inability to inhibit adjacent finger movements while performing the task was infrequent in young adults (2.9% of individuals between 20 and 39 years of age) but increased with age (23.3% between the ages of 40 and 59; 31.0% between ages 60 and 80). Females and males did not differ in their inability to inhibit adjacent finger movements, but individuals with a college education showed a lower frequency of failure to inhibit adjacent finger movements (10.3%) compared to those with a high school education (28.6%). These findings were statistically significant only for the dominant hand.

Conclusion:

Selective motor inhibition failures are most common in the dominant hand and occur primarily in older healthy adults while performing the modified version of the HFTT. Monitoring selective motor inhibition failures may have diagnostic significance.

Keywords

Kinematic recordingsSelective motor inhibitionHalstead Finger Tapping TestAgeSexEducation
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 27 , Issue 8 , September 2021 , pp. 813 - 824
Copyright
Copyright © INS. Published by Cambridge University Press, 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Albers, M.W., Gilmore, G.C., Kaye, J., Murphy, C., Wingfield, A., Bennett, D.A., … Devanand, D.P. (2015). At the interface of sensory and motor dysfunctions and Alzheimer’s disease. Alzheimer’s & Dementia, 11(1), 70–98. doi: 10.1016/j.jalz.2014.04.514 Google Scholar
Aoki, T., Shinohara, M., & Kinoshita, H. (2009). Motor control of individual fingers. In Shinohara, M. (Ed.), Advances in neuromuscular physiology of motor skills and muscle fatigue (pp. 1–24): Thiruvananthapuram: Research Signpost.Google Scholar
Arenaza-Urquijo, E.M., Landeau, B., La Joie, R., Mevel, K., Mézenge, F., Perrotin, A., … Chételat, G. (2013). Relationships between years of education and gray matter volume, metabolism and functional connectivity in healthy elders. Neuroimage, 83, 450–457.CrossRefGoogle ScholarPubMed
Arias, P., Robles-García, V., Corral-Bergantiños, Y., Madrid, A., Espinosa, N., Valls-Solé, J., … Cudeiro, J. (2015). Central fatigue induced by short-lasting finger tapping and isometric tasks: A study of silent periods evoked at spinal and supraspinal levels. Neuroscience, 305, 316–327.CrossRefGoogle ScholarPubMed
Bächinger, M., Rea Lehner, F.T., Hanimann, S., Balsters, J., & Wenderoth, N. (2019). Human motor fatigability as evoked by repetitive movements results from a gradual breakdown of surround inhibition. eLife, 16, 8. doi: 10.7554/eLife.46750 Google Scholar
Beck, S., & Hallett, M. (2011). Surround inhibition in the motor system. Experimental Brain Research, 210(2), 165–172.Google ScholarPubMed
Bedard, A.-C., Nichols, S., Barbosa, J.A., Schachar, R., Logan, G.D., & Tannock, R. (2002). The development of selective inhibitory control across the life span. Developmental Neuropsychology, 21(1), 93–111.CrossRefGoogle ScholarPubMed
Birchenall, J., Térémetz, M., Roca, P., Lamy, J.-C., Oppenheim, C., Maier, M.A., … Lindberg, P.G. (2019). Individual recovery profiles of manual dexterity, and relation to corticospinal lesion load and excitability after stroke – A longitudinal pilot study. Neurophysiologie Clinique, 49(2), 149–164.CrossRefGoogle ScholarPubMed
Booth, J.R., Burman, D.D., Meyer, J.R., Lei, Z., Trommer, B.L., Davenport, N.D., … Mesulam, M.M. (2003). Neural development of selective attention and response inhibition. Neuroimage, 20(2), 737–751.Google ScholarPubMed
Buchman, A.S., & Bennett, D.A. (2011). Loss of motor function in preclinical Alzheimer’s disease. Expert Review of Neurotherapeutics, 11(5), 665–676. doi: 10.1586/ern.11.57 CrossRefGoogle ScholarPubMed
Cohen, J. (1988). Statistical Power Analysis for the Behavioral Sciences. Hillsdale, NJ: L. Erlbaum Associates.Google Scholar
Coxon, J.P., Stinear, C.M., & Byblow, W.D. (2007). Selective inhibition of movement. Journal of Neurophysiology, 97(3), 2480–2489.CrossRefGoogle Scholar
Dehaene, S., Pegado, F., Braga, L.W., Ventura, P., Nunes Filho, G., Jobert, A., … Cohen, L. (2010). How learning to read changes the cortical networks for vision and language. Science, 330(6009), 1359–1364.CrossRefGoogle Scholar
Donald, M. (1991). Origins of the modern mind: Three stages in the evolution of culture and cognition. Cambridge: Harvard University Press.Google Scholar
Dupan, S.S., Stegeman, D.F., & Maas, H. (2018). Distinct neural control of intrinsic and extrinsic muscles of the hand during single finger pressing. Human Movement Science, 59, 223–233.CrossRefGoogle ScholarPubMed
Emerson, R.W., & Cantlon, J.F. (2012). Early math achievement and functional connectivity in the fronto-parietal network. Developmental Cognitive Neuroscience, 2, S139–S151.CrossRefGoogle ScholarPubMed
Häger-Ross, C., & Schieber, M.H. (2000). Quantifying the independence of human finger movements: Comparisons of digits, hands, and movement frequencies. Journal of Neuroscience, 20(22), 8542–8550.CrossRefGoogle ScholarPubMed
Halstead, W.C. (1947). Brain and intelligence: A quantitative study of the frontal lobes. Chicago: The University of Chicago Press.Google Scholar
Hausmann, M., Kirk, I.J., & Corballis, M.C. (2004). Influence of task complexity on manual asymmetries. Cortex, 40(1), 103–110.CrossRefGoogle ScholarPubMed
Hiraoka, K., Ito, S., Lutton, M., Nakano, M., & Yonei, N. (2020). Long-term practice of isolated finger movements reduces enslaved response of tonically contracting little finger abductor to tonic index finger abduction. Experimental Brain Research, 238(2), 499–512.CrossRefGoogle Scholar
Jones, L.A. & Lederman, S.J. (2006). Human hand function. New York: Oxford University Press.Google Scholar
Kim, J., Chey, J., Kim, S.-E., & Kim, H. (2015). The effect of education on regional brain metabolism and its functional connectivity in an aged population utilizing positron emission tomography. Neuroscience Research, 94, 50–61.CrossRefGoogle Scholar
King, B., Van Ruitenbeek, P., Leunissen, I., Cuypers, K., Heise, K.-F., Santos Monteiro, T., … Swinnen, S.P. (2017). Age-related declines in motor performance are associated with decreased segregation of large-scale resting state brain networks. Cerebral Cortex, 28(12), 4390–4402. doi: 10.1093/cercor/bhx297 CrossRefGoogle Scholar
Leckliter, I.N., & Matarazzo, J.D. (1989). The influence of age, education, IQ, gender, and alcohol abuse on Halstead-Reitan neuropsychological test battery performance. Journal of Clinical Psychology, 45(4), 484–512.Google ScholarPubMed
Levin, O., Fujiyama, H., Boisgontier, M.P., Swinnen, S.P., & Summers, J.J. (2014). Aging and motor inhibition: a converging perspective provided by brain stimulation and imaging approaches. Neuroscience & Biobehavioral Reviews, 43, 100–117.CrossRefGoogle ScholarPubMed
Lezak, M.D., Howieson, D.B., Loring, D.W., & Fischer, J.S. (2004). Neuropsychological Assessment (4th ed.). New York: Oxford University Press, USA.Google Scholar
López-Barroso, D., de Schotten, M.T., Morais, J., Kolinsky, R., Braga, L.W., Guerreiro-Tauil, A., … Cohen, L. (2020). Impact of literacy on the functional connectivity of vision and language related networks. Neuroimage, 116722.CrossRefGoogle ScholarPubMed
Mollica, M.A., Tort-Merino, A., Navarra, J., Fernández-Prieto, I., Valech, N., Olives, J., … Sánchez-Valle, R. (2019). Early detection of subtle motor dysfunction in cognitively normal subjects with amyloid-β positivity. Cortex, 121, 117–124.CrossRefGoogle ScholarPubMed
Moore, R.D., Gallea, C., Horovitz, S.G., & Hallett, M. (2012). Individuated finger control in focal hand dystonia: An fMRI study. Neuroimage, 61(4), 823–831.CrossRefGoogle ScholarPubMed
O’Boyle, M.W. Gill, H. Benbow, C. & Alexander, J. (1994). Concurrent finger-tapping in mathematically gifted males: Evidence for enhanced right hemisphere involvement during linguistic processing. Cortex, 30(3), 519–526.CrossRefGoogle ScholarPubMed
Oxford Grice, K., Vogel, K.A., Le, V., Mitchel, A., Muniz, S., & Vollmer, M.A. (2003). Adult norms for a commercially available Nine Hole Peg Test for finger dexterity. American Journal of Occupational Therapy, 57, 570–573.Google ScholarPubMed
Pauwels, L., Maes, C., Hermans, L., & Swinnen, S.P. (2019). Motor inhibition efficiency in healthy aging: the role of γ-aminobutyric acid. Neural Regeneration Research, 14(5), 741.CrossRefGoogle ScholarPubMed
Prigatano, G.P., & Borgaro, S.R. (2003). Qualitative features of finger movement during the Halstead finger oscillation test following traumatic brain injury. Journal of the International Neuropsychological Society, 9(1), 128–133.CrossRefGoogle ScholarPubMed
Prigatano, G.P., Goncalves, C.W.P., de Oliveira, S.B., Denucci, S.M., Pereira, R.M., & Braga, L.W. (2019). Kinematic recordings while performing a modified version of the Halstead Finger Tapping Test: Age, sex, and education effects. Journal of Clinical and Experimental Neuropsychology, 42(2), 1–13. doi: 10.1080/13803395.2019.1665170 Google ScholarPubMed
Prigatano, G.P., & Grant, I. (1988). Neuropsychological correlates of COPD. In McSweeny, A.J. & Grant, I. (Eds.), Chronic obstructive pulmonary disease: a behavioral perspective (Vol. 36, pp. 39–57). New York: Marcel Dekker, Inc.Google Scholar
Prigatano, G.P., Gray, J.A., & Legacy, J. (2008). Predictors of quantitative and qualitative Halstead finger-tapping scores in low socioeconomic status school-age children. Child Neuropsychology, 14(3), 263–276.CrossRefGoogle ScholarPubMed
Prigatano, G.P., & Hoffman, B. (1997). Finger tapping and brain dysfunction: A qualitative and quantitative study. BNI Quarterly, 13. Retrieved from https://www.barrowneuro.org/education/grand-rounds-publications-and-media/barrow-quarterly/volume-13-no-4-1997/finger-tapping-brain-dysfunction-qualitative-quantitative-study/ Google Scholar
Raghavan, P., Petra, E., Krakauer, J.W., & Gordon, A.M. (2006). Patterns of impairment in digit independence after subcortical stroke. Journal of Neurophysiology, 95(1), 369–378.CrossRefGoogle ScholarPubMed
Roalf, D.R., Rupert, P., Mechanic-Hamilton, D., Brennan, L., Duda, J.E., Weintraub, D., … Moberg, P.J. (2018). Quantitative assessment of finger tapping characteristics in mild cognitive impairment, Alzheimer’s disease, and Parkinson’s disease. Journal of Neurology, 265(6), 1365–1375.CrossRefGoogle ScholarPubMed
Rojkova, K., Volle, E., Urbanski, M., Humbert, F., Dell’Acqua, F., & De Schotten, M.T. (2016). Atlasing the frontal lobe connections and their variability due to age and education: a spherical deconvolution tractography study. Brain Structure and Function, 221(3), 1751–1766.CrossRefGoogle ScholarPubMed
Ruitenberg, M.F., Cassady, K.E., Reuter-Lorenz, P., Tommerdahl, M., & Seidler, R.D. (2019). Age-related reductions in tactile and motor inhibitory function start early but are independent. Frontiers in Aging Neuroscience, 11, 193.CrossRefGoogle ScholarPubMed
Seidler, R.D., Bernard, J.A., Burutolu, T.B., Fling, B.W., Gordon, M.T., Gwin, J.T., … Lipps, D.B. (2010). Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neuroscience & Biobehavioral Reviews, 34(5), 721–733.CrossRefGoogle ScholarPubMed
Shin, H.-W., Sohn, Y.H., & Hallett, M. (2009). Hemispheric asymmetry of surround inhibition in the human motor system. Clinical Neurophysiology, 120(4), 816–819.CrossRefGoogle ScholarPubMed
Singh, T., SKM, V., Zatsiorsky, V.M., & Latash, M.L. (2010). Fatigue and motor redundancy: Adaptive increase in finger force variance in multi-finger tasks. Journal of Neurophysiology, 103(6), 2990–3000.CrossRefGoogle ScholarPubMed
Sohn, Y.H., & Hallett, M. (2004). Surround inhibition in human motor system. Experimental Brain Research, 158(4), 397–404.CrossRefGoogle ScholarPubMed
Tallet, J., Albaret, J.-M., & Barral, J. (2013). Developmental changes in lateralized inhibition of symmetric movements in children with and without Developmental Coordination Disorder. Research in Developmental Disabilities, 34(9), 2523–2532.CrossRefGoogle ScholarPubMed
Térémetz, M., Colle, F., Hamdoun, S., Maier, M.A., & Lindberg, P.G. (2015). A novel method for the quantification of key components of manual dexterity after stroke. Journal of Neuroengineering and Rehabilitation, 12(1), 64.CrossRefGoogle ScholarPubMed
Thiebaut de Schotten, M., Cohen, L., Amemiya, E., Braga, L.W., & Dehaene, S. (2014). Learning to read improves the structure of the arcuate fasciculus. Cerebral Cortex, 24, 989–995. doi: 10.1093/cercor/bhs383 CrossRefGoogle ScholarPubMed
Westlye, L.T., Walhovd, K.B., Dale, A.M., Bjørnerud, A., Due-Tønnessen, P., Engvig, A., … Fjell, A.M. (2009). Life-span changes of the human brain white matter: diffusion tensor imaging (DTI) and volumetry. Cerebral Cortex, 20(9), 2055–2068.CrossRefGoogle ScholarPubMed