Younger adult brain utilizes interhemispheric strategy of recruiting ipsilateral dorsal premotor cortex for complex finger movement, but not aging brain

Abstract

The ipsilateral sensorimotor cortices (dorsal premotor cortex [PMd], primary motor cortex [M1], primary somatosensory cortex [S1], and superior parietal cortex of Area 2) are often activated when the healthy younger and older adult brains perform complex finger movements. Prompted by clinical evidence that the ipsilateral PMd plays particularly important roles to complement the movements after stroke, we tested whether the ipsilateral PMd also plays particularly important (complementary) roles among the ipsilateral sensorimotor cortices when healthy younger adults perform a complex motor task by augmenting interhemispheric functional connectivity with the contralateral sensorimotor cortices. We also examined possible strategic difference when older adults with degraded interhemispheric inhibition perform the complex task when compared to younger adults with mature one. We addressed these questions by measuring brain activity with functional magnetic resonance imaging while healthy right-handed younger and older adults performed simple (button pressing with the right index finger) and complex (stick rotation requiring coordination between the right fingers) motor tasks. In younger group, the ipsilateral PMd, S1, Area 2 activated during the complex task, while the ipsilateral M1 remained deactivated as in the simple task, suggesting an existence of interregional difference. The ipsilateral PMd and S1/Area 2 more activated in the individuals with less dexterous performance. The anterior ipsilateral PMd enhanced interhemispheric functional coupling consistently with all of the contralateral sensorimotor cortices during the complex task. In contrast, in older group, all of the ipsilateral cortices including the M1 activated during the complex task, however, none of the cortices showed performance-related activity change. Increase in functional connectivity within the contralateral sensorimotor cortices rather than interhemispheric connectivity was observed during the complex task. The results suggest the importance and complementary role of the ipsilateral PMd for complex finger movement in the younger brains, and the strategic difference (interhemispheric vs. intrahemispheric) when the younger and aging brains perform the movement.

Theoretical proposal for restoration of hand motor function utilizing plasticity of motor-cortical interhemispheric interaction

“…On the other hand, when young adults perform complex unilateral movements (e.g. stick-spinning or ball rotation with multiple fingers), there is activity in the ipsilateral motor cortex (especially in the PMD) in addition to the contralateral activity (Loibl et al, 2011; Uehara et al, 2012; Miura et al, 2024). Thus, the human brain adaptively controls movement by flexibly and plastically altering interhemispheric inhibition between the two motor cortices.…”

“…When young adults perform simple unilateral movements (e.g. simple button pressing with a finger or simple hand alternating extension-flexion movement), the contralateral motor cortex is usually activated, and the ipsilateral motor cortex inhibited (Morita et al, 2019, 2021, 2023; Miura et al, 2024), probably due to interhemispheric inhibition between the two motor cortices (Mullinger et al, 2014). On the other hand, when young adults perform complex unilateral movements (e.g.…”