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

Abstract

Detecting and correcting errors is essential to successful action. Studies on response monitoring have examined scalp ERPs following the commission of motor slips in speeded‐response tasks, focusing on a frontocentral negativity (i.e., error‐related negativity or ERN). Sensorimotor neurophysiologists investigating cortical monitoring of reactive balance recovery behavior observe a strikingly similar pattern of scalp ERPs following externally imposed postural errors, including a brief frontocentral negativity that has been referred to as the balance N1. We integrate and review relevant literature from these discrepant fields to suggest shared underlying mechanisms and potential benefits of collaboration across fields. Unlike the cognitive tasks leveraged to study the ERN, balance perturbations afford precise experimental control of postural errors to elicit balance N1s that are an order of magnitude larger than the ERN and drive robust and well‐characterized adaptation of behavior within an experimental session. Many factors that modulate the ERN, including motivation, perceived consequences, perceptual salience, expectation, development, and aging, are likewise known to modulate the balance N1. We propose that the ERN and balance N1 reflect common neural activity for detecting errors. Collaboration across fields could help clarify the functional significance of the ERN and poorly understood interactions between motor and cognitive impairments.

Classification of Rhythmic Cortical Activity Elicited by Whole-Body Balance Perturbations Suggests the Cortical Representation of Direction-Specific Changes in Postural Stability

“…The low-frequency rhythms may represent the detection of a mismatch between expected and (imposed changes to) current postural stability, which has been previously considered a form of error detection or processing of sensorimotor conflict [4,6,9,10]. This interpretation is consistent with a view of the theta rhythm as representing mechanisms of cognitive control for the self-regulation of behavior [31][32][33][34][35][36].…”

“…The cortical responses to balance perturbations appear in the electroencephalogram (EEG) between 30 and 400 ms after perturbation onset, with a broad scalp distribution and a rich spectral composition [4][5][6]. The cortical responses may reflect concurrent cognitive and sensorimotor processes related to the integration of the multisensory input (visual, vestibular, and proprioceptive) associated with sudden postural changes [7,8] and to the detection of a mismatch between expected and current postural stability, as a form of error detection [9,10] or sensorimotor conflict [4]. In turn, the later cortical responses could represent direct contributions to the reactive postural responses [2,3].…”

“…The broad spatial distribution of the theta enhancement suggests cortico-cortical interactions that may support the integration of sensory information. Second, a transient enhancement of theta, alpha (8)(9)(10)(11)(12), and beta (13)(14)(15)(16)(17) Hz) rhythms appears in midline central cortical areas following physical perturbations [4,5] and in parietal T.S.E., D.dK, and V.W. are with the Department of Rehabilitation, Donders Institute for Brain, Cognition and Behavior, Radboud University Medical Center, (route 932) Postbus 9101, 6500 HB Nijmegen, The Netherlands (correspondence: teodoro.solisescalante@radboudumc.nl).…”

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

“…It has been considered that N1 represents neural processing of sensory information necessary for coordinating reactive balance responses (Dietz et al 1984(Dietz et al , 1985Dimitrov et al 1996;Quant et al 2004;Staines et al 2001;Payne et al 2018;Payne and Ting 2020a). Moreover, it might represent an error signal for postural instability (Adkin et al 2006(Adkin et al , 2008Mochizuki et al 2009;Payne et al 2019). Such sensory information processing might contribute to enhancing the muscle activations of SO and MG that were initiated by the spinal stretch reflexes, since the N1 potential was followed by large activations of SO and MG (Fig.…”

“…One considers that N1 represents neural processing of sensory information (Dietz et al 1984;Dimitrov et al 1996;Staines et al 2001) necessary for coordinating reactive balance responses based on the fact that the latency and amplitude of N1 are altered by the afferent transmission delay (Dietz et al 1985) and the level of cognitive load (Quant et al 2004). Another interpretation is that N1 represents an error signal for detecting postural instability (Adkin et al 2006(Adkin et al , 2008Mochizuki et al 2009;Payne et al 2019). Payne et al have been working to characterize the N1 and other ERPs during perturbed stance in recent years.…”