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Dual-task performance of speech and motor skill: verb generation facilitates grasping behaviour

Abstract

Pronouncing nouns or verbs while grasping distinctly alters movement. Changes in hand speed and final position occur according to the meaning of the words spoken. These results are typically found when executing a single movement paired with a single word. For example, pronouncing the word ‘fast’ increased the speed of the hand when reaching to grasp. Our objective was to compare how verb and noun fluency tasks interact with grasping behaviour in a grasp-to-construct task. Because previous imaging research shows that verb and noun production activates distinct neural areas, we reasoned that grasping outcomes would differ according to the category of word produced by participants. Specifically, we hypothesized that verb pronunciation would distinctly affect grasping behaviour compared to producing nouns. We recruited 38 young adults who performed a grasp-to-construct task and two different verbal fluency tasks. Participants completed each task (grasp, verb fluency, and noun fluency) separately as control conditions, and the grasping and each speaking task simultaneously for dual-task conditions. We found that during the dual-task condition, when generating nouns and grasping, participants made significantly more grasping errors (inaccurate grasps) compared to the control and verb dual-task conditions. Moreover, our results revealed a relationship between the number of verbs generated and grasping performance. Participants who generated more verbs were faster and more accurate during the motor component of the dual-task condition. This relationship was not observed when nouns were produced, indicating a unique relationship between verb production and functional grasping. The result is a facilitation effect, diminishing the negative outcome on motor control associated with increased cognitive load (as observed during noun pronunciation).

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References

  1. Albinet C, Tomporowski PD, Beasman K (2006) Aging and concurrent task performance: cognitive demand and motor control. Educ Gerontol 32(9):689–706. https://doi.org/10.1080/03601270600835421

  2. Alcock KJ, Krawczyk K (2010) Individual differences in language development: relationship with motor skill at 21 months. Dev Sci 13(5):677–691. https://doi.org/10.1111/j.1467-7687.2009.00924.x

  3. Berthier ML, Pulvermüller F (2011) Neuroscience insights improve neurorehabilitation of poststroke aphasia. Nat Rev Neurol 7(2):86

  4. Bishop DV (2002) Motor immaturity and specific speech and language impairment: evidence for a common genetic basis. Am J Med Genet 114(1):56–63

  5. Bocanegra Y, García AM, Pineda D, Buriticá O, Villegas A, Lopera F et al (2015) Syntax, action verbs, action semantics, and object semantics in Parkinson's disease: dissociability, progression, and executive influences. Cortex 69:237–254

  6. Canessa N, Borgo F, Cappa SF, Perani D, Falini A, Buccino G et al (2007) The different neural correlates of action and functional knowledge in semantic memory: an FMRI study. Cereb Cortex 18(4):740–751

  7. Casado P, Martín-Loeches M, León I, Hernández-Gutiérrez D, Espuny J, Muñoz F et al (2018) When syntax meets action: brain potential evidence of overlapping between language and motor sequencing. Cortex 100:40–51

  8. da Silva RL, Labrecque D, Caromano FA, Higgins J, Frak V (2018) Manual action verbs modulate the grip force of each hand in unimanual or symmetrical bimanual tasks. PLoS ONE 13(2):e0192320

  9. Damasio AR, Tranel D (1993) Nouns and verbs are retrieved with differently distributed neural systems. Proc Natl Acad Sci 90(11):4957–4960

  10. Diamond A, Lee K (2011) Interventions shown to aid executive function development in children 4 to 12 years old. Science 333(6045):959–964

  11. Fargier R, Menoret M, Boulenger V, Nazir TA, Paulignan Y (2012) Grasp it loudly! Supporting actions with semantically congruent spoken action words. PLoS ONE 7(1):11. https://doi.org/10.1371/journal.pone.0030663

  12. Frak V, Nazir T, Goyette M, Cohen H, Jeannerod M (2010) Grip force is part of the semantic representation of manual action verbs. PLoS ONE 5(3):5. https://doi.org/10.1371/journal.pone.0009728

  13. Fuller RL, Van Winkle EP, Anderson KE, Gruber-Baldini AL, Hill T, Zampieri C et al (2013) Dual task performance in Parkinson's disease: a sensitive predictor of impairment and disability. Parkinson Relat Disord 19(3):325–328

  14. Garcia AM, Ibanez A (2016) A touch with words: Dynamic synergies between manual actions and language. Neurosci Biobehav Rev 68:59–95. https://doi.org/10.1016/j.neubiorev.2016.04.022

  15. Glover S, Rosenbaum DA, Graham J, Dixon P (2004) Grasping the meaning of words. Exp Brain Res 154(1):103–108. https://doi.org/10.1007/s00221-003-1659-2

  16. Gonzalez CL, Mills KJ, Genee I, Li F, Piquette N, Rosen N, Gibb R (2014a) Getting the right grasp on executive function. Front Psychol 5:285

  17. Gonzalez CL, Li F, Mills KJ, Rosen N, Gibb RL (2014b) Speech in action: degree of hand preference for grasping predicts speech articulation competence in children. Front Psychol 5:1267

  18. Gunduz Can R, Schack T, Koester D (2017) Movement interferes with visuospatial working memory during the encoding: an ERP study. Front Psychol. https://doi.org/10.3389/fpsyg.2017.00871

  19. Harrison JE, Buxton P, Husain M, Wise R (2000) Short test of semantic and phonological fluency: normal performance, validity and test-retest reliability. Br J Clin Psychol 39(2):181–191

  20. Hauk O, Johnsrude I, Pulvermüller F (2004) Somatotopic representation of action words in human motor and premotor cortex. Neuron 41(2):301–307

  21. Hill EL (2001) Non-specific nature of specific language impairment: a review of the literature with regard to concomitant motor impairments. Int J Lang Commun Disord 36(2):149–171

  22. Ibáñez A, Cardona JF, Dos Santos YV, Blenkmann A, Aravena P, Roca M et al (2013) Motor-language coupling: direct evidence from early Parkinson’s disease and intracranial cortical recordings. Cortex 49(4):968–984

  23. IBM SPSS Statistics for Windows (Version Version 23.0.). (Released 2013.). IBM Corp, Armonk

  24. Jeannerod M, Arbib MA, Rizzolatti G, Sakata H (1995) Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci 18(7):314–320. https://doi.org/10.1016/0166-2236(95)93921-J

  25. Knecht S, Dräger B, Deppe M, Bobe L, Lohmann H, Flöel A et al (2000) Handedness and hemispheric language dominance in healthy humans. Brain 123(12):2512–2518

  26. Kolb B, Whishaw IQ (2001) An introduction to brain and behavior. Worth, New York

  27. Kolb B, Whishaw IQ (2009) Fundamentals of human neuropsychology. Macmillan, New York

  28. Leonard HC, Bedford R, Pickles A, Hill EL, Basis Team (2015) Predicting the rate of language development from early motor skills in at-risk infants who develop autism spectrum disorder. Res Autism Spectr Disord 13:15–24

  29. Maas E, Gildersleeve-Neumann CE, Jakielski KJ, Stoeckel R (2014) Motor-based intervention protocols in treatment of childhood apraxia of speech (CAS). Curr Dev Disord Rep 1(3):197–206

  30. McDowd J, Hoffman L, Rozek E, Lyons KE, Pahwa R, Burns J, Kemper S (2011) Understanding verbal fluency in healthy aging, Alzheimer's disease, and Parkinson's disease. Neuropsychology 25(2):210

  31. Mkrtychian N, Blagovechtchenski E, Kurmakaeva D, Gnedykh D, Kostromina S, Shtyrov YY (2019) Concrete vs abstract semantics: from mental representations to functional brain mapping. Front Hum Neurosci 13:267

  32. Moseley RL, Pulvermüller F (2014) Nouns, verbs, objects, actions, and abstractions: local fMRI activity indexes semantics, not lexical categories. Brain Lang 132:28–42

  33. Oliveri M, Finocchiaro C, Shapiro K, Gangitano M, Caramazza A, Pascual-Leone A (2004) All talk and no action: a transcranial magnetic stimulation study of motor cortex activation during action word production. J Cogn Neurosci 16(3):374–381

  34. Östberg P, Fernaeus S-E, Hellström Å, Bogdanović N, Wahlund L-O (2005) Impaired verb fluency: a sign of mild cognitive impairment. Brain Lang 95(2):273–279

  35. Parks RW, Loewenstein DA, Dodrill KL, Barker WW, Yoshii F, Chang JY et al (1988) Cerebral metabolic effects of a verbal fluency test: A PET scan study. J Clin Exp Neuropsychol 10(5):565–575. https://doi.org/10.1080/01688638808402795

  36. Patel P, Lamar M, Bhatt T (2014) Effect of type of cognitive task and walking speed on cognitive-motor interference during dual-task walking. Neuroscience 260:140–148

  37. Péran P, Cardebat D, Cherubini A, Piras F, Luccichenti G, Peppe A et al (2009) Object naming and action-verb generation in Parkinson's disease: a fMRI study. Cortex 45(8):960–971. https://doi.org/10.1016/j.cortex.2009.02.019

  38. Rechetnikov RP, Maitra K (2009) Motor impairments in children associated with impairments of speech or language: a meta-analytic review of research literature. Am J Occup Ther 63(3):255

  39. Repetto C, Colombo B, Cipresso P, Riva G (2013) The effects of rTMS over the primary motor cortex: the link between action and language. Neuropsychologia 51(1):8–13

  40. RStudio Team (2016) RStudio: integrated development for R. RStudio, Inc., Boston, MA URL https://www.rstudio.com/

  41. Salmazo-Silva H, Parente MA, Rocha MS, Baradel RR, Cravo AM, Sato JR, Godinho F, Carthery-Goulart MT (2017) Lexical-retrieval and semantic memory in Parkinson’s disease: the question of noun and verb dissociation. Brain Lang 165:10–20

  42. Shao Z, Janse E, Visser K, Meyer AS (2014) What do verbal fluency tasks measure? Predictors of verbal fluency performance in older adults. Front Psychol 5:772

  43. Shapiro KA, Mottaghy FM, Schiller NO, Poeppel TD, Flüß MO, Müller HW et al (2005) Dissociating neural correlates for nouns and verbs. NeuroImage 24(4):1058–1067. https://doi.org/10.1016/j.neuroimage.2004.10.015

  44. Shapiro KA, Moo LR, Caramazza A (2006) Cortical signatures of noun and verb production. Proc Natl Acad Sci 103(5):1644–1649

  45. Silveri MC, Traficante D, Monaco MRL, Iori L, Sarchioni F, Burani C (2018) Word selection processing in Parkinson's disease: When nouns are more difficult than verbs. Cortex 100:8–20

  46. Stone KD, Gonzalez CL (2015) Manual preferences for visually-and haptically-guided grasping. Acta Physiol (Oxf) 160:1–10

  47. Stone KD, Bryant DC, Gonzalez CL (2013) Hand use for grasping in a bimanual task: evidence for different roles? Exp Brain Res 224(3):455–467

  48. Suggate SP, Stoeger H (2014) Do nimble hands make for nimble lexicons? Fine motor skills predict knowledge of embodied vocabulary items. First Lang 34(3):244–261. https://doi.org/10.1177/0142723714535768

  49. Suggate SP, Stoeger H (2017) Fine motor skills enhance lexical processing of embodied vocabulary: a test of the nimble-hands, nimble-minds hypothesis. Q J Exp Psychol 70(10):2169–2187

  50. Tomasino B, Fink GR, Sparing R, Dafotakis M, Weiss PH (2008) Action verbs and the primary motor cortex: a comparative TMS study of silent reading, frequency judgments, and motor imagery. Neuropsychologia 46(7):1915–1926

  51. Vainio L, Schulman M, Tiippana K, Vainio M (2013) Effect of syllable articulation on precision and power grip performance. PLoS ONE 8(1):10. https://doi.org/10.1371/journal.pone.0053061

  52. Vainio L, Tiainen M, Tiippana K, Komeilipoor N, Vainio M (2015) Interaction in planning movement direction for articulatory gestures and manual actions. Exp Brain Res 233(10):2951–2959

  53. Vigliocco G, Vinson DP, Druks J, Barber H, Cappa SF (2011) Nouns and verbs in the brain: a review of behavioural, electrophysiological, neuropsychological and imaging studies. Neurosci Biobehav Rev 35(3):407–426. https://doi.org/10.1016/j.neubiorev.2010.04.007

  54. Warburton E, Wise RJ, Price CJ, Weiller C, Hadar U, Ramsay S, Frackowiak RS (1996) Noun and verb retrieval by normal subjects studies with PET. Brain 119(1):159–179

  55. Weigelt M, Rosenbaum DA, Huelshorst S, Schack T (2009) Moving and memorizing: motor planning modulates the recency effect in serial and free recall. Acta Physiol (Oxf) 132(1):68–79. https://doi.org/10.1016/j.actpsy.2009.06.005

  56. Wilson M (2002) Six views of embodied cognition. Psychon Bull Rev 9(4):625–636

  57. Woods SP, Scott JC, Sires DA, Grant I, Heaton RK, Tröster AI, HIV Neurobehavioral Research Center (HNRC) Group (2005) Action (verb) fluency: test–retest reliability, normative standards, and construct validity. J Int Neuropsychol Soc 11(4):408–415

  58. Yan JH, Zhou CL (2009) Effects of motor practice on cognitive disorders in older adults. Eur Rev Aging Phys Act 6(2):67

  59. Zhang Z, Sun Y, Wang Z (2018) Representation of action semantics in the motor cortex and Broca’s area. Brain Lang 179:33–41. https://doi.org/10.1016/j.bandl.2018.02.003

  60. Zhao Q, Guo Q, Hong Z (2013) Clustering and switching during a semantic verbal fluency test contribute to differential diagnosis of cognitive impairment. Neurosci Bull 29(1):75–82

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Correspondence to Nicole van Rooteselaar.

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van Rooteselaar, N., Beke, C. & Gonzalez, C.L.R. Dual-task performance of speech and motor skill: verb generation facilitates grasping behaviour. Exp Brain Res 238, 453–463 (2020). https://doi.org/10.1007/s00221-020-05725-x

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Keywords

  • Grasp-to-construct
  • Verb generation
  • Noun generation
  • Facilitation
  • Dual task
  • Speech production