Age Interferes with Sensorimotor Timing and Error Correction in the Supra-second Range

Overview

Journal Front Aging Neurosci

Specialty Geriatrics

Date 2023 Jan 27

PMID 36704500

Authors

Bettina Pollok

Amelie Hagedorn

Vanessa Krause

Sonja A Kotz

Affiliations

Soon will be listed here.

Abstract

Introduction: Precise motor timing including the ability to adjust movements after changes in the environment is fundamental to many daily activities. Sensorimotor timing in the sub-and supra-second range might rely on at least partially distinct brain networks, with the latter including the basal ganglia (BG) and the prefrontal cortex (PFC). Since both structures are particularly vulnerable to age-related decline, the present study investigated whether age might distinctively affect sensorimotor timing and error correction in the supra-second range.

Methods: A total of 50 healthy right-handed volunteers with 22 older (age range: 50-60 years) and 28 younger (age range: 20-36 years) participants synchronized the tap-onsets of their right index finger with an isochronous auditory pacing signal. Stimulus onset asynchronies were either 900 or 1,600 ms. Positive or negative step-changes that were perceivable or non-perceivable were occasionally interspersed to the fixed intervals to induce error correction. A simple reaction time task served as control condition.

Results And Discussion: In line with our hypothesis, synchronization variability in trials with supra-second intervals was larger in the older group. While reaction times were not affected by age, the mean negative asynchrony was significantly smaller in the elderly in trials with positive step-changes, suggesting more pronounced tolerance of positive deviations at older age. The analysis of error correction by means of the phase correction response (PCR) suggests reduced error correction in the older group. This effect emerged in trials with supra-second intervals and large positive step-changes, only. Overall, these results support the hypothesis that sensorimotor synchronization in the sub-second range is maintained but synchronization accuracy and error correction in the supra-second range is reduced in the elderly as early as in the fifth decade of life suggesting that these measures are suitable for the early detection of age-related changes of the motor system.

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References

Ivry R . The representation of temporal information in perception and motor control. Curr Opin Neurobiol. 1996; 6(6):851-7. DOI: 10.1016/s0959-4388(96)80037-7. View

Pollok B, Jurkiewicz M, Krause V . Anodal Transcranial Direct Current Stimulation (atDCS) of the Primary Motor Cortex (M1) Facilitates Nonconscious Error Correction of Negative Phase Shifts. Neural Plast. 2022; 2022:9419154. PMC: 9159881. DOI: 10.1155/2022/9419154. View

Raz N, Gunning F, Head D, Dupuis J, McQuain J, Briggs S . Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter. Cereb Cortex. 1997; 7(3):268-82. DOI: 10.1093/cercor/7.3.268. View

Wiener M, Turkeltaub P, Coslett H . The image of time: a voxel-wise meta-analysis. Neuroimage. 2009; 49(2):1728-40. DOI: 10.1016/j.neuroimage.2009.09.064. View

Niessen E, Fink G, Hoffmann H, Weiss P, Stahl J . Error detection across the adult lifespan: Electrophysiological evidence for age-related deficits. Neuroimage. 2017; 152:517-529. DOI: 10.1016/j.neuroimage.2017.03.015. View

Kotz S, Schwartze M . Cortical speech processing unplugged: a timely subcortico-cortical framework. Trends Cogn Sci. 2010; 14(9):392-9. DOI: 10.1016/j.tics.2010.06.005. View

Lewis P, Miall R . Distinct systems for automatic and cognitively controlled time measurement: evidence from neuroimaging. Curr Opin Neurobiol. 2003; 13(2):250-5. DOI: 10.1016/s0959-4388(03)00036-9. View

Mangels J, Ivry R, Shimizu N . Dissociable contributions of the prefrontal and neocerebellar cortex to time perception. Brain Res Cogn Brain Res. 1998; 7(1):15-39. DOI: 10.1016/s0926-6410(98)00005-6. View

Raz N, Lindenberger U, Rodrigue K, Kennedy K, Head D, Williamson A . Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex. 2005; 15(11):1676-89. DOI: 10.1093/cercor/bhi044. View

10.

Nieuwenhuis S, Ridderinkhof K, Talsma D, Coles M, Holroyd C, Kok A . A computational account of altered error processing in older age: dopamine and the error-related negativity. Cogn Affect Behav Neurosci. 2002; 2(1):19-36. DOI: 10.3758/cabn.2.1.19. View

11.

Turgeon M, Wing A . Late onset of age-related difference in unpaced tapping with no age-related difference in phase-shift error detection and correction. Psychol Aging. 2012; 27(4):1152-63. DOI: 10.1037/a0029925. View

12.

Grady C, Springer M, Hongwanishkul D, McIntosh A, Winocur G . Age-related changes in brain activity across the adult lifespan. J Cogn Neurosci. 2006; 18(2):227-41. DOI: 10.1162/089892906775783705. View

13.

Grahn J . Neural mechanisms of rhythm perception: current findings and future perspectives. Top Cogn Sci. 2012; 4(4):585-606. DOI: 10.1111/j.1756-8765.2012.01213.x. View

14.

Mates J, Muller U, Radil T, Poppel E . Temporal integration in sensorimotor synchronization. J Cogn Neurosci. 2013; 6(4):332-40. DOI: 10.1162/jocn.1994.6.4.332. View

15.

Thaut M, Stephan K, Wunderlich G, Schicks W, Tellmann L, Herzog H . Distinct cortico-cerebellar activations in rhythmic auditory motor synchronization. Cortex. 2008; 45(1):44-53. DOI: 10.1016/j.cortex.2007.09.009. View

16.

Hoffmann S, Falkenstein M . Aging and error processing: age related increase in the variability of the error-negativity is not accompanied by increase in response variability. PLoS One. 2011; 6(2):e17482. PMC: 3046248. DOI: 10.1371/journal.pone.0017482. View

17.

Lockhart S, DeCarli C, Fama R . Neuroimaging of the aging brain: introduction to the special issue of neuropsychology review. Neuropsychol Rev. 2014; 24(3):267-70. PMC: 4262518. DOI: 10.1007/s11065-014-9269-2. View

18.

Koch G, Oliveri M, Torriero S, Caltagirone C . Underestimation of time perception after repetitive transcranial magnetic stimulation. Neurology. 2003; 60(11):1844-6. DOI: 10.1212/wnl.60.11.1844. View

19.

Pardo J, Lee J, Sheikh S, Surerus-Johnson C, Shah H, Munch K . Where the brain grows old: decline in anterior cingulate and medial prefrontal function with normal aging. Neuroimage. 2007; 35(3):1231-7. PMC: 1913629. DOI: 10.1016/j.neuroimage.2006.12.044. View

20.

Petter E, Lusk N, Hesslow G, Meck W . Interactive roles of the cerebellum and striatum in sub-second and supra-second timing: Support for an initiation, continuation, adjustment, and termination (ICAT) model of temporal processing. Neurosci Biobehav Rev. 2016; 71:739-755. DOI: 10.1016/j.neubiorev.2016.10.015. View