Functional segregation of cortical hand and speech areas by frequency detuning of an intrinsic motor rhythm

Many decades after Penfield's (Penfield W, Boldrey E. Brain 60: 389-443, 1937) classic depiction of the motor homunculus, it remains unclear how spatially contiguous and interconnected representations within human sensorimotor cortex might separate their activities to achieve the directed and precise control of distinct body regions evident in activities as different as typing and speaking. One long-standing but relatively neglected explanation draws from models of simple physical systems (like swinging pendulums) to posit that small differences in the oscillatory properties of neuronal populations (termed "frequency detuning") can result in highly effective segregation of their activities and outputs. We tested this hypothesis by comparing the peak frequencies of beta-band (13-30 Hz) motor rhythms measured in a magnetoencephalographic neuroimaging study of finger and speech movements in a group of healthy adults and a group of typically developing children. Our results confirm a peak frequency task difference (speech movement vs. hand movement) of about 1.5 Hz in the beta motor rhythms of both left and right hemispheres in adults. A comparable task difference was obtained in children for the left but not for the right hemisphere. These results provide novel support for the role of frequency detuning in the functional organization of the brain and suggest that this mechanism should play a more prominent role in current models of bodily representations and their development within the sensorimotor cortex.NEW & NOTEWORTHY This work is the first evidence for frequency detuning of an intrinsic motor rhythm in spatially contiguous regions of primary motor cortex associated with hand and speech movements, supporting a mechanism of functional segregation that has been largely overlooked by current models of motor cortex organization. Our results from children further provide the first evidence for frequency detuning in the developing brain, indicating an early-developing mechanism with later refinements of hemispheric control.