Top-down modulation of brain activity underlying intentional action and its relationship with awareness of intention: an ERP/Laplacian analysis

Abstract

Intentional actions are executed with the peculiar experience of "I decide to do that." It has been proposed that intentional actions involve a specific brain network involving the supplementary motor areas (SMAs). Here, we manipulated the internal representation participants attended to (intention vs. movement) in order to (1) examine the activity of SMAs and of the primary motor cortex (M1) during intentional action preparation and execution, and (2) investigate the temporal relationship between activity in these structures and intention awareness. Participants performed self-paced key presses. After each key press, participants were asked to report either the time they had the first intention to press the key (W-condition) or the time they actually started the movement (M-condition). We then estimated surface Laplacians from brain electrical potentials recorded while participants were performing the task. Activity in SMAs was greater in the W-condition than in the M-condition more than 1 s before electromyographic (EMG) activation, suggesting that this region is indeed associated to the formation of conscious intention. Conversely, activity in primary motor cortex (M1) contralateral to the responding hand was larger in the M-condition than in the W-condition, revealing that this region is also modulated by top-down processes. In addition, waveforms time-locked to the W-judgement revealed that M1 as well as EMG activation preceded the time at which participants become aware of their intention by about 0.3 s. This observation argues against the possibility that the temporal delay between motor-related activation and intention awareness results from smearing artifacts.

Disentangling Neural Sources of the Motor Interference Effect in High Functioning Autism: An EEG-Study

“…This suggests that a participant's action intention affected early visual processing of the observed action, indicating an influence of action on perception. Third, we found a congruency-related difference in the Readiness Potential (RP; with the spatial resolution of the EEG-signal increased by means of Laplacian transformations; Rigoni et al, 2013;Tandonnet et al, 2005;Vidal et al, 2003, see also Methods). This is a component which typically magnifies with increasing complexities of motor preparation (Rigoni, Brass, Roger, Vidal, & Sartori, 2013;Tandonnet, Burle, Hasbroucq, & Vidal, 2005;Vidal, Grapperon, Bonnet, & Hasbroucq, 2003).…”

“…For the N190, we focused on the time window from 190 to 210 ms, and for the left N190, we pooled the activity per condition at left hemispheric electrodes 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 P5, P7 and PO7; for the right N190, we pooled the activity per condition at the right hemispheric electrodes P6, P8 and PO8. For the stimulus-locked P3, we pooled the activity at electrodes CPz, Pz and POz per condition in the time window from 350 to 400 ms. Based on earlier research (Leuthold & Schröter, 2011;Rigoni et al, 2013;Shibasaki & Hallett, 2006), we identified the RP component in the response-locked segments as the gradient shift preceding the steep negative slope before response onset at electrode FCz (i.e., from -400 to -100 ms for the current dataset). To disentangle the activity of the supplementary motor area, related to motor preparation processes, from contaminating activity related to motor execution processes in the M1, we increased the spatial resolution of the EEG-signal by means of Laplacian transformations (Rigoni et al, 2013;Tandonnet et al, 2005;Vidal et al, 2003).…”

“…For the stimulus-locked P3, we pooled the activity at electrodes CPz, Pz and POz per condition in the time window from 350 to 400 ms. Based on earlier research (Leuthold & Schröter, 2011;Rigoni et al, 2013;Shibasaki & Hallett, 2006), we identified the RP component in the response-locked segments as the gradient shift preceding the steep negative slope before response onset at electrode FCz (i.e., from -400 to -100 ms for the current dataset). To disentangle the activity of the supplementary motor area, related to motor preparation processes, from contaminating activity related to motor execution processes in the M1, we increased the spatial resolution of the EEG-signal by means of Laplacian transformations (Rigoni et al, 2013;Tandonnet et al, 2005;Vidal et al, 2003). Due to the poor spatial resolution of the EEG-signal, volume conduction effects smear the distribution of the potentials at the scalp level, therefore producing overlapping effects of motor execution and motor preparation processes within the RP (Rigoni et al, 2013).…”

“…To disentangle the activity of the supplementary motor area, related to motor preparation processes, from contaminating activity related to motor execution processes in the M1, we increased the spatial resolution of the EEG-signal by means of Laplacian transformations (Rigoni et al, 2013;Tandonnet et al, 2005;Vidal et al, 2003). Due to the poor spatial resolution of the EEG-signal, volume conduction effects smear the distribution of the potentials at the scalp level, therefore producing overlapping effects of motor execution and motor preparation processes within the RP (Rigoni et al, 2013). The Laplacian transformation removes the blurring effect of the diffusion of currents through the skull and acts as a high-pass filter.…”

“…First, we interpolated the signal with the spherical spline interpolation procedure, and then computed second derivatives in the two dimensions of the space (degree of spline = 3, maximum degrees the Legendre Polynomial = 15. Conform earlier studies (e.g., Rigoni et al, 2013;Vidal et al, 2003) and the observed topography (figure 2), we conducted the RP-analyses on electrode FCz.…”