Greater neural responses to trajectory errors are associated with superior force field adaptation in older adults

Abstract

Although age-related declines in cognitive, sensory and motor capacities are well documented, current evidence is mixed as to whether or not aging impairs sensorimotor adaptation to a novel dynamic environment. More importantly, the extent to which any deficits in sensorimotor adaptation are due to general impairments in neural plasticity, or impairments in the specific processes that drive adaptation is unclear. Here we investigated whether there are age-related differences in electrophysiological responses to reaching endpoint and trajectory errors caused by a novel force field, and whether markers of error processing relate to the ability of older adults to adapt their movements. Older and young adults (N = 24/group, both sexes) performed 600 reaches to visual targets, and received audio-visual feedback about task success or failure after each trial. A velocity-dependent curl field pushed the hand to one side during each reach. We extracted ERPs time-locked to movement onset [kinematic error-related negativity (kERN)], and the presentation of success/failure feedback [feedback error-related negativity (fERN)]. At a group level, older adults did not differ from young adults in the rate or extent of sensorimotor adaptation, but EEG responses to both trajectory errors and task errors were reduced in the older group. Most interestingly, the amplitude of the kERN correlated with the rate and extent of sensorimotor adaptation in older adults. Thus, older adults with an impaired capacity for encoding kinematic trajectory errors also have compromised abilities to adapt their movements in a novel dynamic environment.

Adaptation of reach action to a novel force-field is not predicted by acuity of dynamic proprioception in either older or younger adults

“…This study adds to the increasing, but still limited, number of reports indicating a minimal effect of ageing on reach adaptation to novel forces (Cesqui et al, 2008;Rajeshkumar & Trewartha, 2019;Reuter et al, 2018;Trewartha et al, 2014). In addition, we demonstrate this finding holds true under conditions of limited visual feedback (providing only distance information during movement, and terminal error), conditions which might emphasize proprioceptive control.…”

“…To perturb proprioceptive feedback specifically, external forces can be applied during discrete targeted movements (Krakauer et al, 1999;Sarlegna et al, 2010;Shadmehr & Mussa-Ivaldi, 1994). Unlike tasks with visual feedback perturbation (Anguera et al, 2011;Bock, 2005;Buch et al, 2003;Contreras-Vidal et al, 2002;Hegele & Heuer, 2010;Seidler, 2006;Vandevoorde & Orban de Xivry, 2019), a number of studies have indicated a minimal role of ageing in the ability to adapt movements to novel force environments (Cesqui et al, 2008;Huang & Ahmed, 2014;Rajeshkumar & Trewartha, 2019;Reuter et al, 2018;Trewartha et al, 2014). Nonetheless, several age-dependent performance predictors have been highlighted, including increased muscle co-contraction (Huang & Ahmed, 2014), reduced central processing of kinematic errors (Reuter et al, 2018) and reduced spatial working memory capacity (Trewartha et al, 2014).…”

“…Unlike tasks with visual feedback perturbation (Anguera et al, 2011;Bock, 2005;Buch et al, 2003;Contreras-Vidal et al, 2002;Hegele & Heuer, 2010;Seidler, 2006;Vandevoorde & Orban de Xivry, 2019), a number of studies have indicated a minimal role of ageing in the ability to adapt movements to novel force environments (Cesqui et al, 2008;Huang & Ahmed, 2014;Rajeshkumar & Trewartha, 2019;Reuter et al, 2018;Trewartha et al, 2014). Nonetheless, several age-dependent performance predictors have been highlighted, including increased muscle co-contraction (Huang & Ahmed, 2014), reduced central processing of kinematic errors (Reuter et al, 2018) and reduced spatial working memory capacity (Trewartha et al, 2014). Furthermore, younger adults demonstrate a tight relationship between proprioceptive perception and motor performance when adapting to novel force-fields (Haith et al, 2008;Mattar et al, 2013;Ohashi et al, 2019;Ostry et al, 2010).…”

“…Moreover, whilst adaptation to forces is possible in younger adults without visual feedback of hand position (Franklin et al, 2007;Lefumat et al, 2015;Scheidt et al, 2005), all previous studies with older adults have included either full (Cesqui et al, 2008;Huang & Ahmed, 2014;Rajeshkumar & Trewartha, 2019;Trewartha et al, 2014) or early visual feedback (first half of the movement; Reuter et al, 2018). Hence, the interactions of age and proprioceptive acuity on dynamic motor adaptation remains poorly understood, and the contributions of visual and proprioceptive feedback to motor adaptation have not been dissociated.…”

Neural Signatures of Reward and Sensory Prediction Error in Motor Learning

“…It has been proposed that the 75 P300 reflects the updating of a model of stimulus context (Donchin and Coles 1988). Both the FRN 76 and the P300 have been observed in response to errors in motor tasks (Krigolson et al 2008; Torrecil-77 los et al 2014;MacLean et al 2015;Reuter et al 2018;Savoie et al 2018) . In this paper we describe 78 experiments in which we isolated and compared EEG responses to both reward and sensory error 79 feedback using separate adaptation paradigms that produced comparable changes in behavior.…”