Explicit Action Switching Interferes with the Context-Specificity of Motor Memories in Older Adults
Carly J Sombric, Harrison M Harker, Patrick J Sparto, Gelsy Torres-Oviedo, Carly J Sombric, Harrison M Harker, Patrick J Sparto, Gelsy Torres-Oviedo
Abstract
Healthy aging impairs the ability to adapt movements to novel situations and to switch choices according to the context in cognitive tasks, indicating resistance to changes in motor and cognitive behaviors. Here we examined if this lack of "flexibility" in old subjects observed in motor and cognitive domains were related. To this end, we evaluated subjects' performance in a motor task that required switching walking patterns and its relation to performance in a cognitive switching task. Specifically, a group of old (>73 years old) and young subjects learned a new locomotor pattern on a split-belt treadmill, which drives the legs at different speeds. In both groups, we assessed the ability to disengage the walking pattern learned on the treadmill when walking overground. Then, we determined if this motor context-specificity was related to subjects' cognitive ability to switch actions in a set-shift task. Motor and cognitive behaviors were tested twice on separate visits to determine if age-related differences were maintained with exposure. Consistent with previous studies, we found that old adults adapted slower and had deficits in retention. Most importantly, we found that older subjects could not switch locomotor patterns when transitioning across walking contexts. Interestingly, cognitive switching performance was inversely related to subjects' ability to switch walking patterns. Thus, cognitive mediated switching interfered with locomotor switching. These findings were maintained across testing sessions. Our results suggest that distinct neural substrates mediate motor and cognitive action selection, and that these processes interfere with each other as we age.
Keywords: aging; generalization; human; locomotion; motor adaptation; motor learning; set-shift; split-belt treadmill.
Figures
References
- Adrover-Roig D., Barceló F. (2010). Individual differences in aging and cognitive control modulate the neural indexes of context updating and maintenance during task switching. Cortex 46, 434–450. 10.1016/j.cortex.2009.09.012
- Albert S. M., Duffy J. (2012). Differences in risk aversion between young and older adults. Neurosci. Neuroecon. 2012, 1–12. 10.2147/nan.s27184
- Anguera J. A., Bernard J. A., Jaeggi S. M., Buschkuehl M., Benson B. L., Jennett S., et al. . (2012). The effects of working memory resource depletion and training on sensorimotor adaptation. Behav. Brain Res. 228, 107–115. 10.1016/j.bbr.2011.11.040
- Anguera J. A., Reuter-Lorenz P. A., Willingham D. T., Seidler R. D. (2011). Failure to engage spatial working memory contributes to age-related declines in visuomotor learning. J. Cogn. Neurosci. 23, 11–25. 10.1162/jocn.2010.21451
- Bäckman L., Nyberg L., Lindenberger U., Li S.-C., Farde L. (2006). The correlative triad among aging, dopamine, and cognition: current status and future prospects. Neurosci. Biobehav. Rev. 30, 791–807. 10.1016/j.neubiorev.2006.06.005
- Balser N., Lorey B., Pilgramm S., Stark R., Bischoff M., Zentgraf K., et al. . (2014). Prediction of human actions: expertise and task-related effects on neural activation of the action observation network. Hum. Brain Mapp. 35, 4016–4034. 10.1002/hbm.22455
- Bierbaum S., Peper A., Karamanidis K., Arampatzis A. (2011). Adaptive feedback potential in dynamic stability during disturbed walking in the elderly. J. Biomech. 44, 1921–1926. 10.1016/j.jbiomech.2011.04.027
- Bo J., Borza V., Seidler R. D. (2009). Age-related declines in visuospatial working memory correlate with deficits in explicit motor sequence learning. J. Neurophysiol. 102, 2744–2754. 10.1152/jn.00393.2009
- Bock O. (2005). Components of sensorimotor adaptation in young and elderly subjects. Exp. Brain Res. 160, 259–263. 10.1007/s00221-004-2133-5
- Bock O., Girgenrath M. (2006). Relationship between sensorimotor adaptation and cognitive functions in younger and older subjects. Exp. Brain Res. 169, 400–406. 10.1007/s00221-005-0153-4
- Boyd L. A., Winstein C. J. (2004). Providing explicit information disrupts implicit motor learning after basal ganglia stroke. Learn. Mem. 11, 388–396. 10.1101/lm.80104
- Brown M. J., Almeida Q. J. (2011). Evaluating dopaminergic system contributions to cued pattern switching during bimanual coordination. Eur. J. Neurosci. 34, 632–640. 10.1111/j.1460-9568.2011.07773.x
- Bruijn S. M., Van Impe A., Duysens J., Swinnen S. P. (2012). Split-belt walking: adaptation differences between young and older adults. J. Neurophysiol. 108, 1149–1157. 10.1152/jn.00018.2012
- Buch E. R., Young S., Contreras-Vidal J. L. (2003). Visuomotor adaptation in normal aging. Learn. Mem. 10, 55–63. 10.1101/lm.50303
- Burge J., Ernst M. O., Banks M. S. (2008). The statistical determinants of adaptation rate in human reaching. J. Vis. 8, 20.1–20.19. 10.1167/8.4.20
- Castro L. N., Hadjiosif A. M., Hemphill M. A., Smith M. A. (2014). Environmental consistency determines the rate of motor adaptation. Curr. Biol. 24, 1050–1061. 10.1016/j.cub.2014.03.049
- Chen T. Y., Peronto C. L., Edwards J. D. (2012). Cognitive function as a prospective predictor of falls. J. Gerontol. 67, 720–728. 10.1093/geronb/gbs052
- Coubard O. A., Duretz S., Lefebvre V., Lapalus P., Ferrufino L. (2011). Practice of contemporary dance improves cognitive flexibility in aging. Front. Aging Neurosci. 3:13. 10.3389/fnagi.2011.00013
- Coxon J. P., Goble D. J., Van Impe A., De Vos J., Wenderoth N., Swinnen S. P. (2010). Reduced basal ganglia function when elderly switch between coordinated movement patterns. Cereb. Cortex 20, 2368–2379. 10.1093/cercor/bhp306
- Criscimagna-Hemminger S. E., Bastian A. J., Shadmehr R. (2010). Size of error affects cerebellar contributions to motor learning. J. Neurophysiol. 103, 2275–2284. 10.1152/jn.00822.2009
- Dreher J. C., Grafman J. (2002). The roles of the cerebellum and basal ganglia in timing and error prediction. Eur. J. Neurosci. 16, 1609–1619. 10.1046/j.1460-9568.2002.02212.x
- Fernández-Ruiz J., Hall C., Vergara P., Díaz R. (2000). Prism adaptation in normal aging: slower adaptation rate and larger aftereffect. Cogn. Brain Res. 9, 223–226. 10.1016/S0926-6410(99)00057-9
- Finley J. M., Bastian A. J., Gottschall J. S. (2013). Learning to be economical: the energy cost of walking tracks motor adaptation. J. Physiol. 591, 1081–1095. 10.1113/jphysiol.2012.245506
- Finley J. M., Long A., Bastian A. J., Torres-Oviedo G. (2015). Spatial and temporal control contribute to step length asymmetry during split-belt adaptation and hemiparetic gait. Neurorehabil. Neural Repair 29, 786–795. 10.1177/1545968314567149
- Fjell A. M., Walhovd K. B. (2010). Structural brain changes in aging: courses, causes and cognitive consequences. Rev. Neurosci. 21, 187–221. 10.1515/REVNEURO.2010.21.3.187
- Friedman D., Nessler D., Johnson R., Ritter W., Bersick M. (2007). Age-related changes in executive function: an Event-Related Potential (ERP) investigation of task-switching. Aging Neuropsychol. Cogn. 15, 95–128. 10.1080/13825580701533769
- Galea J. M., Vazquez A., Pasricha N., de Xivry J. J., Celnik P. (2011). Dissociating the roles of the cerebellum and motor cortex during adaptive learning: the motor cortex retains what the cerebellum learns. Cereb. Cortex 21, 1761–1770. 10.1093/cercor/bhq246
- Goble D. J., Coxon J. P., Wenderoth N., Van Impe A., Swinnen S. P. (2009). Proprioceptive sensibility in the elderly: degeneration, functional consequences and plastic-adaptive processes. Neurosci. Biobehav. Rev. 33, 271–278. 10.1016/j.neubiorev.2008.08.012
- Gualtieri C. T., Johnson L. G. (2006). Reliability and validity of a computerized neurocognitive test battery, CNS vital signs. Arch. Clin. Neuropsychol. 21, 623–643. 10.1016/j.acn.2006.05.007
- Gualtieri C. T., Johnson L. G. (2008). Age-related cognitive decline in patients with mood disorders. Prog. Neuropsychopharmacol. Biol. Psychiatry 32, 962–967. 10.1016/j.pnpbp.2007.12.030
- Hegele M., Heuer H. (2010). Adaptation to a direction-dependent visuomotor gain in the young and elderly. Psychol. Res. 74, 21–34. 10.1007/s00426-008-0221-z
- Hegele M., Heuer H. (2013). Age-related variations of visuomotor adaptation result from both the acquisition and the application of explicit knowledge. Psychol. Aging 28, 333–339. 10.1037/a0031914
- Heuer H., Hegele M. (2008). Adaptation to visuomotor rotations in younger and older adults. Psychol. Aging 23, 190–202. 10.1037/0882-7974.23.1.190
- Heuer H., Hegele M. (2011). Generalization of implicit and explicit adjustments to visuomotor rotations across the workspace in younger and older adults. J. Neurophysiol. 106, 2078–2085. 10.1152/jn.00043.2011
- Holloszy J. O., Larsson L. (1995). Motor units: remodeling in aged animals. J. Gerontol. A Biol. Sci. Med. Sci. 50, 91–95. 10.1093/gerona/50A.Special_Issue.91
- Huang H. J., Ahmed A. A. (2014). Older adults learn less, but still reduce metabolic cost, during motor adaptation. J. Neurophysiol. 111, 135–144. 10.1152/jn.00401.2013
- Huang V. S., Shadmehr R. (2009). Persistence of motor memories reflects statistics of the learning event. J. Neurophysiol. 102, 931–940. 10.1152/jn.00237.2009
- Inzelberg R., Plotnik M., Flash T., Schechtman E., Shahar I., Korczyn A. D. (2001). Mental and motor switching in Parkinson's disease. J. Mot. Behav. 33, 377–385. 10.1080/00222890109601921
- Izawa J., Criscimagna-Hemminger S. E., Shadmehr R. (2012). Cerebellar contributions to reach adaptation and learning sensory consequences of action. J. Neurosci. 32, 4230–4239. 10.1523/JNEUROSCI.6353-11.2012
- Kallio J., Søgaard K., Avela J., Komi P., Selänne H., Linnamo V. (2012). Age-related decreases in motor unit discharge rate and force control during isometric plantar flexion. J. Electromyogr. Kinesiol. 22, 983–989. 10.1016/j.jelekin.2012.05.009
- Klassen J., Tong C., Flanagan J. R. (2005). Learning and recall of incremental kinematic and dynamic sensorimotor transformations. Exp. Brain Res. 164, 250–259. 10.1007/s00221-005-2247-4
- Klein C., Fischer B., Hartnegg K., Heiss W. H., Roth M. (2000). Optomotor and neuropsychological performance in old age. Exp. Brain Res. 135, 141–154. 10.1007/s002210000506
- Klouda L., Franklin W. J., Saraf A., Parekh D. R., Schwartz D. D. (2017). Neurocognitive and executive functioning in adult survivors of congenital heart disease. Congenit. Heart Dis. 12, 91–98. 10.1111/chd.12409
- Kluzik J., Diedrichsen J., Shadmehr R., Bastian A. J. (2008). Reach adaptation: what determines whether we learn an internal model of the tool or adapt the model of our arm? J. Neurophysiol. 100, 1455–1464. 10.1152/jn.90334.2008
- Körding K. P., Wolpert D. M. (2004). Bayesian integration in sensorimotor learning. Nature 427, 244–247. 10.1038/nature02169
- Korenberg A. T., Ghahramani Z. (2002). A Bayesian view of motor adaptation. Curr. Psychol. Cogn. 21, 537–564.
- Kramer A. F., Humphrey D. G., Larish J. F., Logan G. D., Strayer D. L. (1994). Aging and inhibition: beyond a unitary view of inhibitory processing in attention. Psychol. Aging 9, 491–512. 10.1037/0882-7974.9.4.491
- Laidlaw D. H., Bilodeau M., Enoka R. M. (2000). Steadiness is reduced and motor unit discharge is more variable in old adults. Muscle Nerve 23, 600–612. 10.1002/(SICI)1097-4598(200004)23:4<600::AID-MUS20>;2-D
- Langan J., Seidler R. D. (2011). Age differences in spatial working memory contributions to visuomotor adaptation and transfer. Behav. Brain Res. 225, 160–168. 10.1016/j.bbr.2011.07.014
- Leunissen I., Coxon J. P., Geurts M., Caeyenberghs K., Michiels K., Sunaert S., et al. . (2013). Disturbed cortico-subcortical interactions during motor task switching in traumatic brain injury. Hum. Brain Mapp. 34, 1254–1271. 10.1002/hbm.21508
- Luft A. R., Skalej M., Schulz J. B., Welte D., Kolb R., Bürk K., et al. . (1999). Patterns of age-related shrinkage in cerebellum and brainstem observed in vivo using three-dimensional MRI volumetry. Cereb. Cortex 9, 712–21. 10.1093/cercor/9.7.712
- Maheu M., Houde M.-S., Landry S. P., Champoux F. (2015). The effects of aging on clinical vestibular evaluations. Front. Neurol. 6:205. 10.3389/fneur.2015.00205
- Malone L. A., Bastian A. J. (2016). Age-related forgetting in locomotor adaptation. Neurobiol. Learn. Mem. 128, 1–6. 10.1016/j.nlm.2015.11.003
- Malone L. A., Bastian A. J. (2010). Thinking about walking: effects of conscious correction versus distraction on locomotor adaptation. J. Neurophysiol. 103, 1954–1962. 10.1152/jn.00832.2009
- Malone L., Bastian A., Torres-Oviedo G. (2012). How does the motor system correct for errors in time and space during locomotor adaptation? J. Neurophysiol. 108, 672–683. 10.1152/jn.00391.2011
- McNay E. C., Willingham D. B. (1998). Deficit in learning of a motor skill requiring strategy, but not of perceptuomotor recalibration, with aging. Learn. Mem. 4, 411–420. 10.1101/lm.4.5.411
- Mitchell R., Curtis K., Watson W. L., Nau T. (2010). Age differences in fall-related injury hospitalisations and trauma presentations. Australas. J. Ageing 29, 117–125. 10.1111/j.1741-6612.2010.00413.x
- Nagengast A. J., Braun D. A., Wolpert D. M. (2010). Risk-sensitive optimal feedback control accounts for sensorimotor behavior under uncertainty. PLoS Comput. Biol. 6:e1000857. 10.1371/journal.pcbi.1000857
- O'Brien M. K., Ahmed A. A. (2015). Threat affects risk preferences in movement decision making. Front. Behav. Neurosci. 9:150. 10.3389/fnbeh.2015.00150
- Odonkor C. A., Thomas J. C., Holt N., Latham N., vanSwearingen J., Brach J. S., et al. . (2013). A comparison of straight- and curved-Path walking tests among mobility-limited older adults. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 68, 1532–1539. 10.1093/gerona/glt060
- Ota M., Yasuno F., Ito H., Seki C., Nozaki S., Asada T., et al. (2006). Age-related decline of dopamine synthesis in the living human brain measured by positron emission tomography with L-[β-11 C] DOPA. Life Sci. 79, 730–736. 10.1016/j.lfs.2006.02.017
- Pauwels L., Vancleef K., Swinnen S. P., Beets I. A. M. (2015). Challenge to promote change: both young and older adults benefit from contextual interference. Front. Aging Neurosci. 7:157. 10.3389/fnagi.2015.00157
- Raz N., Lindenberger U., Rodrigue K. M., Kennedy K. M., Head D., Williamson A., et al. . (2005). Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb. Cortex 15, 1676–1689. 10.1093/cercor/bhi044
- Reisman D. S., Block H. J., Bastian A. J. (2005). Interlimb coordination during locomotion: what can be adapted and stored? J. Neurophysiol. 94, 2403–2415. 10.1152/jn.00089.2005
- Rodrigue K. M., Kennedy K. M., Raz N. (2005). Aging and longitudinal change in perceptual-motor skill acquisition in healthy adults. J. Gerontol. B Psychol. Sci. Soc. Sci. 60, P174–P181. 10.1093/geronb/60.4.p174
- Schweighofer N., Lee J.-Y., Goh H.-T., Choi Y., Kim S. S., Stewart J. C., et al. . (2011). Mechanisms of the contextual interference effect in individuals poststroke. J. Neurophysiol. 106, 2632–2641. 10.1152/jn.00399.2011
- Seidler R. D. (2006). Differential effects of age on sequence learning and sensorimotor adaptation. Brain Res. Bull. 70, 337–346. 10.1016/j.brainresbull.2006.06.008
- Seidler R. D. (2007). Older adults can learn to learn new motor skills. Behav. Brain Res. 183, 118–122. 10.1016/j.bbr.2007.05.024
- Shadmehr R., Brashers-Krug T. (1997). Functional stages in the formation of human long-term motor memory. J. Neurosci. 17, 409–419.
- Smith M. A., Ghazizadeh A., Shadmehr R. (2006). Interacting adaptive processes with different timescales underlie short-term motor learning. PLoS Biol. 4:e179. 10.1371/journal.pbio.0040179
- Talbot L. A., Musiol R. J., Witham E. K., Metter E. J. (2005). Falls in young, middle-aged and older community dwelling adults: perceived cause, environmental factors and injury. BMC Public Health 5:86. 10.1186/1471-2458-5-86
- Torres-Oviedo G., Bastian A. J. (2010). Seeing is believing: effects of visual contextual cues on learning and transfer of locomotor adaptation. J. Neurosci. 30, 17015–17022. 10.1523/JNEUROSCI.4205-10.2010
- Torres-Oviedo G., Bastian A. J. (2012). Natural error patterns enable transfer of motor learning to novel contexts. J. Neurophysiol. 107, 346–356. 10.1152/jn.00570.2011
- Trent M. C., Ahmed A. A. (2013). Learning from the value of your mistakes: evidence for a risk-sensitive process in movement adaptation. Front. Comput. Neurosci. 7:118. 10.3389/fncom.2013.00118
- Trewartha K. M., Garcia A., Wolpert D. M., Flanagan J. R. (2014). Fast but fleeting: adaptive motor learning processes associated with aging and cognitive decline. J. Neurosci. 34, 13411–13421. 10.1523/JNEUROSCI.1489-14.2014
- Tymula A., Rosenberg Belmaker L. A., Ruderman L., Glimcher P. W., Levy I. (2013). Like cognitive function, decision making across the life span shows profound age-related changes. Proc. Natl. Acad. Sci. U.S.A. 110, 17143–17148. 10.1073/pnas.1309909110
- Tyrell C. M., Helm E., Reisman D. S. (2014). Learning the spatial features of a locomotor task is slowed after stroke. J. Neurophysiol. 112, 480–489. 10.1152/jn.00486.2013
- Van Asselen M., Ridderinkhof K. R. (2000). Shift costs of predictable and unexpected set shifting in young and older adults. Psychol. Belg. 40, 259–273.
- Vanden Noven M. L., Pereira H. M., Yoon T., Stevens A. A., Nielson K. A., Hunter S. K. (2014). Motor variability during sustained contractions increases with cognitive demand in older adults. Front. Aging Neurosci. 6:97. 10.3389/fnagi.2014.00097
- Vasudevan E. V. L., Torres-oviedo G., Morton S. M., Yang J. F., Bastian A. J. (2011). Younger is not always better: development of locomotor adaptation from childhood to adulthood. J. Neurosci. 31, 3055–3065. 10.1523/JNEUROSCI.5781-10.2011
- Wang J., Przybyla A., Wuebbenhorst K., Haaland K. Y., Sainburg R. L. (2011). Aging reduces asymmetries in interlimb transfer of visuomotor adaptation. Exp. Brain Res. 210, 283–290. 10.1007/s00221-011-2631-1
- Wei K., Körding K. (2009). Relevance of error: what drives motor adaptation? J. Neurophysiol. 101, 655–664. 10.1152/jn.90545.2008
- Wei K., Körding K. (2010). Uncertainty of feedback and state estimation determines the speed of motor adaptation. Front. Comput. Neurosci. 4:11. 10.3389/fncom.2010.00011
- Wolpert D. M., Ghahramani Z., Jordan M. I. (1995). An internal model for sensorimotor integration. Science 269, 1880–1882. 10.1126/science.7569931
- Wolpert D. M., Kawato M. (1998). Multiple paried forward and inverse models for motor control. Neural Netw. 11, 1317–1329. 10.1016/S0893-6080(98)00066-5
- Zhang C., Hua T., Li G., Tang C., Sun Q., Zhou P. (2008). Visual function declines during normal aging. Curr. Sci. 95, 1544–1550.
Source: PubMed