Abstract
Previous studies in non-human primates (NHPs) have shown that beta oscillations (15–30 Hz) of local field potentials (LFPs) in the arm/hand areas of primary motor cortex (MI) propagate as traveling waves across the cortex. These waves exhibited two stereotypical features across animals and tasks: (1) The waves propagated in two dominant modal directions roughly 180° apart, and (2) their propagation speed ranged from 10 to 35 cm/s. It is, however, unknown if such cortical waves occur in the human motor cortex. This study shows that the two properties of propagating beta waves are present in MI of a tetraplegic human patient while he was instructed to perform an instruction delay center-out task using a cursor controlled by the chin. Moreover, we show that beta waves are sustained and have similar properties whether the subject was engaged in the task or at rest. The directions of the successive sustained waves both in the human subject and a NHP subject tended to switch from one dominant mode to the other, and at least in the NHP subject the estimated distance traveled between successive waves traveling into and out of the central sulcus is consistent with the hypothesis of wave reflection between the border of motor and somatosensory cortices. Further, we show that the occurrence of the beta waves is not uniquely tied to periods of increased power in the beta frequency band. These results demonstrate that traveling beta waves in MI are a general phenomenon occurring in human as well as NHPs. Consistent with the NHP data, the dominant directions of the beta LFP waves in human aligned to the proximal to distal gradient of joint representations in MI somatotopy. This consistent finding of wave propagation may imply the existence of a hardwired organization of motor cortex that mediates this spatiotemporal pattern.
Highlights
Beta oscillations (10–35 Hz) of local field potentials (LFPs) have been observed in various parts of the brain including primary motor (MI), somatosensory (S1, areas 2 and 3a), and posterior parietal cortices in the neocortex and subcortical areas such basal ganglia and cerebellum (Sanes and Donoghue, 1993; Murthy and Fetz, 1996a,b; Courtemanche and Lamarre, 2005; Witham and Baker, 2007; Witham et al, 2007; Kuhn et al, 2008)
We tested three specific hypotheses: (1) Do beta waves exist in MI of a tetraplegic patient having weak afferent and efferent connections between motor cortex and the periphery? (2). Do they exhibit similar properties to those observed in non-human primate (NHP)? (3) What kind of dynamics governs changes in directions of successive beta waves? We show that (1) beta waves do exist in MI of the human subject whether he was engaged in a task or at rest and are not directly tied to periods of increased beta power
The spatiotemporal dynamics of beta LFP oscillations in MI of a tetraplegic human subject were found to propagate as planar waves whose statistical properties were consistent with those observed in NHPs (Rubino et al, 2006; Takahashi and Hatsopoulos, 2007; Hatsopoulos et al, 2010)
Summary
Beta oscillations (10–35 Hz) of local field potentials (LFPs) have been observed in various parts of the brain including primary motor (MI), somatosensory (S1, areas 2 and 3a), and posterior parietal (area 5) cortices in the neocortex and subcortical areas such basal ganglia and cerebellum (Sanes and Donoghue, 1993; Murthy and Fetz, 1996a,b; Courtemanche and Lamarre, 2005; Witham and Baker, 2007; Witham et al, 2007; Kuhn et al, 2008) Beta oscillations increase their amplitude during movement planning, attenuate at the start of movement, and rebound once a movement is completed (Sanes and Donoghue, 1993; Murthy and Fetz, 1996a,b; Donoghue et al, 1998; Jurkiewicz et al, 2006; Keinrath et al, 2006; O’Leary and Hatsopoulos, 2006). The statistical properties of wave propagation are quite similar during spontaneous and evoked periods
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