Dissociation of muscle and cortical response scaling to balance perturbation acceleration

Abstract

The role of cortical activity in standing balance is unclear. Here we tested whether perturbation-evoked cortical responses share sensory input with simultaneous balance-correcting muscle responses. We hypothesized that the acceleration-dependent somatosensory signals that drive the initial burst of the muscle automatic postural response also drive the simultaneous perturbation-evoked cortical N1 response. We measured in healthy young adults ( n = 16) the initial burst of the muscle automatic postural response (100–200 ms), startle-related muscle responses (100–200 ms), and the perturbation-evoked cortical N1 potential, i.e., a negative peak in cortical EEG activity (100–200 ms) over the supplementary motor area. Forward and backward translational support-surface balance perturbations were applied at four levels of acceleration and were unpredictable in timing, direction, and acceleration. Our results from averaged and single-trial analyses suggest that although cortical and muscle responses are evoked by the same perturbation stimulus, their amplitudes are independently modulated. Although both muscle and cortical responses increase with acceleration, correlations between single-trial muscle and cortical responses were very weak. Furthermore, across subjects, the scaling of muscle responses to acceleration did not correspond to scaling of cortical responses to acceleration. Moreover, we observed a reduction in cortical response amplitude across trials that was related to a reduction in startle-related—but not balance-correcting—muscle activity. Therefore, cortical response attenuation may be related to a reduction in perceived threat rather than motor adaptation or changes in sensory inflow. We conclude that the cortical N1 reflects integrated sensory inputs simultaneously related to brain stem-mediated balance-correcting muscle responses and startle reflexes. NEW & NOTEWORTHY Reactive balance recovery requires sensory inputs to be transformed into appropriate balance-correcting motor responses via brain stem circuits; these are accompanied by simultaneous and poorly understood cortical responses. We used single-trial analyses to dissociate muscle and cortical response modulation with perturbation acceleration. Although muscle and cortical responses share sensory inputs, they have independent scaling mechanisms. Attenuation of cortical responses with experience reflected attenuation of brain stem-mediated startle responses rather than the amplitude of balance-correcting motor responses.

Long-lasting event-related beta synchronizations of electroencephalographic activity in response to support-surface perturbations during upright stance

“…As in the previous study (Quant et al 2005;Payne et al 2018; Payne and Ting 2020a), the ERPs of P1, N1, P2 and N2 were confirmed around the Cz electrode ( Fig. 1I and 3-top).…”

“…Payne et al have been working to characterize the N1 and other ERPs during perturbed stance in recent years. They showed that: (1) people with lower balance ability exhibited larger N1 responses compared to those with better balance control (Payne and Ting 2020a); and (2) N1 includes startle responses in addition to balancecorrecting motor responses (Payne et al 2018). In addition, they also showed abnormal N2 activity in PD patients (Payne and Ting 2020b), where N2 is induced with a latency of about 400 ms with much smaller amplitudes compared to N1, suggesting that later components might be less reflexive and more supraspinal-network-dependent.…”

Do sensorimotor perturbations to standing balance elicit an error‐related negativity?

“…In addition to error‐related and error‐correcting muscle activity, balance perturbations elicit error‐related cortical activity resembling the ERN (Figure ). Specifically, a frontocentral negativity called the balance N1 is evoked simultaneous to the balance‐correcting muscle activity (Payne, Hajcak, & Ting, ). The balance N1 is a negative peak of cortical activity occurring between 100–200 ms after balance perturbation at frontal and central midline EEG electrodes (Fz, FCz, Cz; Marlin et al, ; Mierau, Hulsdunker, & Struder, ), with amplitudes large enough to observe on single trials (Mierau et al, ; Payne et al, ).…”

“…Specifically, a frontocentral negativity called the balance N1 is evoked simultaneous to the balance‐correcting muscle activity (Payne, Hajcak, & Ting, ). The balance N1 is a negative peak of cortical activity occurring between 100–200 ms after balance perturbation at frontal and central midline EEG electrodes (Fz, FCz, Cz; Marlin et al, ; Mierau, Hulsdunker, & Struder, ), with amplitudes large enough to observe on single trials (Mierau et al, ; Payne et al, ). The balance N1 has been localized to the supplementary motor area (Marlin et al, ; Mierau et al, ), but theories of its function are extremely limited.…”

“…Larger and more intense balance perturbations elicit a larger balance N1 response (Mochizuki et al, ; Payne et al, ; Staines et al, ). Likewise, the ERN increases in amplitude with the extent of an error, such as when an error is committed with both the wrong finger and the wrong hand compared to errors committed with either the wrong finger or the wrong hand (Bernstein, Scheffers, & Coles, ).…”