Evidence for a motor gamma-band network governing response interference

Abstract

The gamma-band response is thought to represent a key neural signature of information processing in the human brain. These brain signals have been associated with a variety of sensory modalities (vision, sensation, and audition) and also following basic motor responses, yet the functional significance of the motor gamma-band response remains unclear. We used the Multi-Source Interference Task (MSIT) to assess the sensitivity of these cortical motor gamma-band rhythms to stimuli producing response interference. We recorded MEG from adult participants (N=24) during MSIT task performance and compared motor gamma-band activity on Control and Interference trials. Reaction time on MSIT Interference trials was significantly longer (~0.2 s) for all subjects. Response interference produced a significant increase in motor gamma-band activity including ~0.5 s sustained increase in gamma-band activity from contralateral primary motor area directly preceding the response. In addition, activation of increased right Inferior Frontal Gyrus (R-IFG) was observed at gamma-band frequencies ~0.2 s prior to the button press response. Post-hoc analysis of R-IFG gamma-band activity was observed to correlate with reaction time increases to response interference. Our study is the first to record MEG during MSIT task performance. We observed novel activity of the motor gamma-band on interference trials which was sustained prior to the response and in novel locations including contralateral (BA6), and R-IFG. Our results support the idea that R-IFG is specialized structure for response control that also functions at gamma-band frequencies. Together, these data provide evidence for a motor gamma-band network for response selection and maintenance of planned behavior.

Fig. 1

An illustration of the Multi-Source Interference Task (MSIT).

Fig. 2

MSIT behavioral response summary. MSIT behavioral measures are shown for Control and Interference trials over all subjects (N=23). Mean reaction time for Control trials was 652.7 ms (130.7 S.D.). The mean reaction time for Interference trials was 857.6 ms (183.3). Error bars show standard deviations.

Fig. 3

The peak locations of the MIc (Control and Interference conditions) for N=23 subjects were thresholded using one sample t-tests at p<0.001 for the Post-Response (0 to 0.3) activation time window. The cross-hairs indicate location MNI [−32 −22 52] precentral gyrus location (Brodmann Area 4; BA4). No significant differences were observed between conditions using paired t-tests and Family-wise error (FEW) correction.

Fig. 4

The peak locations of the MIc (Control and Interference conditions) for N=23 subjects were thresholded using one sample t-tests at p<0.0005 for the Pre-Response (−0.3 s to 0) activation time window. A significant difference was observed between conditions (paired t-test (FEW corrected)) to precentral motor areas (BA6). A significant activation of R-IFG was also observed (p<0.05; paired t-test (FEW corrected)).

Fig. 5

Time–frequency analysis of source activity from BA6 locations are shown for Control and Interference trials. Interference trials are associated with an increase in gamma-band power from contralateral (left hemisphere) BA6∼0.6 s (50–75 Hz band) prior to response at time=0 s (p<0.05 corrected). Ipsilateral (right hemisphere) BA6 gamma-band activity is also increased on Interference trials, starting ∼−0.6 s prior to button press response, and persists for ∼0.3 s Post-Response (p−.05 corrected). A between condition beta-band ERD difference was also observed (lower panel) which mainly occurred ∼−0.6 to −0.4 s prior to the response and which likely reflects the between-condition difference in mean reaction time.

Fig. 6

a. Shows the location of R-IFG activity (p<0.05; paired t-test FWE corrected) indicated by cross-hairs. b.Time–frequency t-map of the difference between conditions based on the R-IFG location. Gamma-band (∼90 Hz) power increases approximately −0.2 s prior to the button press response. c. The between-condition time–frequency difference was assessed over the 60–90Hz range and for the Pre-Response time period (−0.3 to 0 s) (shown in the black box). A significant correlation (p=0.034) was observed between the difference in gamma power (Interference–Control) and the difference in RT (Interference–Control) from R-IFG. These results indicate that individuals with relatively longer responses to Interference stimuli showed relatively more gamma-band power from R-IFG.