Ageing increases reliance on sensorimotor prediction through structural and functional differences in frontostriatal circuits

Abstract

The control of voluntary movement changes markedly with age. A critical component of motor control is the integration of sensory information with predictions of the consequences of action, arising from internal models of movement. This leads to sensorimotor attenuation—a reduction in the perceived intensity of sensations from self-generated compared with external actions. Here we show that sensorimotor attenuation occurs in 98% of adults in a population-based cohort (n=325; 18–88 years; the Cambridge Centre for Ageing and Neuroscience). Importantly, attenuation increases with age, in proportion to reduced sensory sensitivity. This effect is associated with differences in the structure and functional connectivity of the pre-supplementary motor area (pre-SMA), assessed with magnetic resonance imaging. The results suggest that ageing alters the balance between the sensorium and predictive models, mediated by the pre-SMA and its connectivity in frontostriatal circuits. This shift may contribute to the motor and cognitive changes observed with age.

Action enhances predicted touch

“…Resolution of these conflicts will be crucial for determining the typical influence of prediction on perception in healthy young populations, as well as older and clinical populations. Tactile attenuation during actionand even more specifically, this particular force judgement paradigmhas been used to demonstrate sensory differences associated with healthy ageing (Wolpe et al, 2016), motor severity in Parkinson's disease (Wolpe et al, 2018) and hallucinatory severity in schizophrenia (Shergill et al, 2014). Such differences are typically attributed to aberrant prediction of action consequences, but a closer inspection is necessary if the underlying mechanisms are not predictive.…”

“…In contrast, typical experiments demonstrating attenuation during action compare the perception of events in the presence or absence of action, or when events are coincident versus delayed with respect to action (e.g. Bays et al, 2005Bays et al, , 2006Blakemore et al, 1998;Kilteni et al, 2019;Kilteni & Ehrsson, 2017;Shergill et al, 2013;Wolpe et al, 2016Wolpe et al, , 2018. In these experiments it is assumed that the sensory events which coincide with action are the (more) predicted consequences, which explains why perception of them is attenuated.…”

“…For example, if we lift a cup of coffee that is lighter than expected, attenuated processing of expected signals (e.g., touch on our fingertips) will allow dedicated processing of unexpected events (e.g., accelerating motion of the cup) to allow swift updating of our beliefs about the environment (e.g., the weight of the cup) and support corrective action to avoid spillage. These downweighting mechanisms are invoked to explain that self-produced tactile sensations generate lower activity in bilateral secondary somatosensory cortex (Blakemore et al, 1998;Kilteni & Ehrsson, 2020;Shergill et al, 2013Shergill et al, , 2014, and are perceived to be less intense (Bays et al, 2005(Bays et al, , 2006Kilteni et al, 2019;Kilteni & Ehrsson, 2017;Shergill et al, 2003;Wolpe et al, 2016Wolpe et al, , 2018, than externallyproduced forces. This theory also provides an explanation for why it is difficult to tickle oneself (Blakemore et al, 1998).…”

Motor planning of vertical arm movements in healthy older adults: does effort optimization persist with aging?

“…showing that sensory attenuation, a well-studied feedforward mechanism (Blakemore et al 1998;Shergill et al 2005;Pareés et al 2014), increases with aging (Wolpe et al 2016).…”

“…There are pieces of evidence suggesting that feedforward mechanisms remain functional with healthy aging and may even compensate for unreliable feedback mechanisms (Boisgontier and Nougier 2013;Wolpe et al 2016;Helsen et al 2016;Hoellinger et al 2017; Vandevoorde and Orban de Xivry 2019). The result that older adults still plan directiondependent arm movements in the gravity field further supports and extends this hypothesis.…”