Development of Right-hemispheric Dominance of Inferior Parietal Lobule in Proprioceptive Illusion Task

Abstract

Functional lateralization can be an indicator of brain maturation. We have consistently shown that, in the adult brain, proprioceptive processing of muscle spindle afferents generating illusory movement of the right hand activates inferior frontoparietal cortical regions in a right-side dominant manner in addition to the cerebrocerebellar motor network. Here we provide novel evidence regarding the development of the right-dominant use of the inferior frontoparietal cortical regions in humans using this task. We studied brain activity using functional magnetic resonance imaging while 60 right-handed blindfolded healthy children (8–11 years), adolescents (12–15 years), and young adults (18–23 years) (20 per group) experienced the illusion. Adult-like right-dominant use of the inferior parietal lobule (IPL) was observed in adolescents, while children used the IPL bilaterally. In contrast, adult-like lateralized cerebrocerebellar motor activation patterns were already observable in children. The right-side dominance progresses during adolescence along with the suppression of the left-sided IPL activity that emerges during childhood. Therefore, the neuronal processing implemented in the adult's right IPL during the proprioceptive illusion task is likely mediated bilaterally during childhood, and then becomes right-lateralized during adolescence at a substantially later time than the lateralized use of the cerebrocerebellar motor system for kinesthetic processing.

Developmental Changes in Task‐Induced Brain Deactivation in Humans Revealed by a Motor Task

“…This developmental period appears to correspond well with the suppression of executive function timing implemented in the ipsilateral M1 by the development of inhibitory systems, such as transcallosal inhibition from the contralateral M1 (Hanakawa et al , ). If the ipsilateral SM1 deactivation is associated with the development of interhemispheric inhibition during the childhood‐to‐adolescence transition, this result is compatible with our previous result showing the emergence of right‐hemispheric dominance in bodily recognition during adolescence by suppressing the activity in the left hemisphere (Naito et al , ). The transition to adolescence appears to be a developmental period when lateralized use of cerebral hemispheres is facilitated for some brain functions (at least for bodily recognition and unimanual movements).…”

“…We then calculated the mean parameter estimate across the participants in each group. Such visualization ensured the validity of our findings in the between‐group comparisons (see also Naito et al , ). Hence, we did not perform any statistical evaluations of the parameter estimation data, thus avoiding the circular evaluation issue raised by Kriegeskorte et al ().…”

“…We also found activation in the right inferior frontal cortex, including the anterior insula, and right inferior parietal cortex. The inferior frontoparietal cortices likely form a network connected by the inferior branch of the superior longitudinal fasciculus, and may perform the function of online monitoring of ongoing actions and sensory experiences (Berti et al , ; Naito et al , ; Morita et al , ). In addition to these regions, we also found activation in the left inferior frontal cortex, including the anterior insula, and left cerebellar hemisphere.…”

“…We used the same procedure for the other deactivation comparisons. The validity of the masking procedure is discussed in our previous papers (Naito et al , ; Morita et al , ).…”

Local-to-distant development of the cerebrocerebellar sensorimotor network in the typically developing human brain: a functional and diffusion MRI study

“…Moreover, it has been demonstrated that 6- to 13-year-old children and adolescents already exhibit activation in the cerebrocerebellar sensorimotor network between the contralateral SM1 and the ipsilateral cerebellar hemisphere (lobules V and VI) when they performed finger-tapping tasks with their right hands, with some quantitative difference from adults (De Guio et al 2012 ; Turesky et al 2018 ). Furthermore, we previously demonstrated that 8- to 11-year-old children recruit the cerebrocerebellar sensorimotor network during kinesthetic (muscle spindle afferent) processing of the right hand (Naito et al 2017 ).…”