Online proprioception feeds plasticity of arm representation following tool-use in healthy aging

Abstract

Following tool-use, the kinematics of free-hand movements are altered. This modified kinematic pattern has been taken as a behavioral hallmark of the modification induced by tool-use on the effector representation. Proprioceptive inputs appear central in updating the estimated effector state. Here we questioned whether online proprioceptive modality that is accessed in real time, or offline, memory-based, proprioception is responsible for this update. Since normal aging affects offline proprioception only, we examined a group of 60 year-old adults for proprioceptive acuity and movement’s kinematics when grasping an object before and after tool-use. As a control, participants performed the same movements with a weight—equivalent to the tool—weight-attached to their wrist. Despite hampered offline proprioceptive acuity, 60 year-old participants exhibited the typical kinematic signature of tool incorporation: Namely, the latency of transport components peaks was longer and their amplitude reduced after tool-use. Instead, we observed no kinematic modifications in the control condition. In addition, online proprioception acuity correlated with tool incorporation, as indexed by the amount of kinematics changes observed after tool-use. Altogether, these findings point to the prominent role played by online proprioception in updating the body estimate for the motor control of tools.

Body schema plasticity is altered in Developmental Coordination Disorder

“…In healthy adults, the explicit representation of the body metrics (or Body Image) has been shown to be largely immune to the effects of tool use. When required to indicate their forearm length using the same paradigm as in the present study, adults' performance shows that the explicit knowledge of their forearm length is not modified after tool use (Bahmad et al, 2020;Cardinali et al, 2011Cardinali et al, , 2012Martel et al, 2019). Yet, this is not the case during development: TD children and adolescents judge their forearm as being shorter after tool use (Martel et al, 2021), a sign of their Body Image plasticity.…”

“…As recalled in the introduction, TD children and early adolescents show a tool-induced kinematic pattern opposite to adults (Baccarini et al, 2014;Bahmad et al, 2020;Cardinali et al, 2009Cardinali et al, , 2011Martel et al, 2019): after tool use, their kinematics display increased peak amplitudes and decreased peak latencies in several parameters of the reaching phase of their free-hand movements, resulting in shorter movement times (Martel et al, 2021). While it is presently uncertain whether it results from vision-biased motor control of tools, or the establishment of new sensorimotor associations (or both), this pattern is consistent with a change in the arm length estimate, in the direction of shortening.…”

Body schema plasticity is altered in Developmental Coordination Disorder

“…In healthy adults, the explicit representation of the body metrics (or body image) has been shown to be largely immune to the effects of tool use. When required to indicate their forearm length using the same paradigm as in the present study, adults performance show that the explicit knowledge of their forearm length is not modified after tool use (Bahmad et al, 2020;Cardinali et al, 2011Cardinali et al, , 2012Martel et al, 2019). Yet, this is not the case during development: TD children and adolescents judge their forearm as being shorter after tool use (Martel et al, 2021).…”

“…As alluded to in the introduction, TD children and early adolescents show a tool-induced kinematic pattern opposite to adults (Baccarini et al, 2014;Bahmad et al, 2020;Cardinali et al, 2009Cardinali et al, , 2011Martel et al, 2019): after tool use, their kinematics display increased peak amplitudes and decreased peak latencies in several parameters of the reach phase of their free-hand movements, resulting in shorter movement times (Martel et al, 2021). While it is presently uncertain whether it results from vision biased motor control of tools, or the establishment of new sensorimotor associations (or both), this pattern is consistent with a change in the arm length estimate in the direction of its shortening.…”

Extending tactile space with hand-held tools: A re-analysis and review

“…In the early 20 th century, the British neurologists Henry Head and Gordon Holmes even noted that our bodily senses of location and movement extend with hand-held instruments (Head & Holmes, 1911). Though it took over eighty years for this claim to begin to be researched empirically (Maravita & Iriki, 2004; Martel, Cardinali, Roy, & Farne, 2016), numerous studies in the last three decades have found that tools influence numerous neurocognitive processes underlying perception (Canzoneri et al, 2013; Cardinali et al, 2011; Miller, Cawley-Bennett, Longo, & Saygin, 2017; Miller, Longo, & Saygin, 2014; Reed, Betz, Garza, & Roberts, 2010; Sposito, Bolognini, Vallar, & Maravita, 2012; Witt, Proffitt, & Epstein, 2005) and action (Bahmad et al, 2020; Berti & Frassinetti, 2000; Biggio, Bisio, Avanzino, Ruggeri, & Bove, 2020; Cardinali, Brozzoli, Finos, Roy, & Farnè, 2016; Cardinali et al, 2009; Farnè, Iriki, & Làdavas, 2005; Ganesh, Yoshioka, Osu, & Ikegami, 2014; Iriki, Tanaka, & Iwamura, 1996; Martel et al, 2019; Umiltà et al, 2008). However, most of this research has focused almost exclusively on the effects of controlling a tool (Johnson-Frey, 2004), ignoring the fact that tools also extend our ability to sense the environment (Vaught, Simpson, & Ryder, 1968).…”