Effortful verb retrieval from semantic memory drives beta suppression in mesial frontal regions involved in action initiation

Abstract

The contribution of the motor cortex to the semantic retrieval of verbs remains a subject of debate in neuroscience. Here, we examined whether additional engagement of the cortical motor system was required when access to verbs semantics was hindered during a verb generation task. We asked participants to produce verbs related to presented noun cues that were either strongly associated with a single verb to prompt fast and effortless verb retrieval, or were weakly associated with multiple verbs and more difficult to respond to. Using power suppression of magnetoencephalography beta oscillations (15–30 Hz) as an index of cortical activation, we performed a whole‐brain analysis in order to identify the cortical regions sensitive to the difficulty of verb semantic retrieval. Highly reliable suppression of beta oscillations occurred 250 ms after the noun cue presentation and was sustained until the onset of verbal response. This was localized to multiple cortical regions, mainly in the temporal and frontal lobes of the left hemisphere. Crucially, the only cortical regions where beta suppression was sensitive to the task difficulty, were the higher order motor areas on the medial and lateral surfaces of the frontal lobe. Stronger activation of the premotor cortex and supplementary motor area accompanied the effortful verb retrieval and preceded the preparation of verbal responses for more than 500 ms, thus, overlapping with the time window of verb retrieval from semantic memory. Our results suggest that reactivation of verb‐related motor plans in higher order motor circuitry promotes the semantic retrieval of target verbs.

On the Boundaries between Decision and Action: Effector-selective Lateralization of Beta-frequency Power Is Modulated by the Lexical Frequency of Printed Words

“…In contrast to the effect of lexical frequency, no effect of action semantics was detected in any of the indexes of motor-response activation. Albeit null results warrant against any strong conclusion, this pattern may be indicative of the boundary conditions for the effect of action semantics on motor-response preparation and implementation (e.g., Klepp et al, 2015;Pavlova, Butorina, Nikolaeva, Prokofyev, Ulanov, Bondarev, & Stroganova, 2019). For example, within semantic tasks requiring the classification of word stimuli as abstract vs concrete, motor-related response-locked attenuation of beta oscillations is reduced for verbs referring to an action performed by the hand, the effector involved in the response (Klepp et al, 2015).…”

Improvement of phonemic fluency following leftward prism adaptation

“…Another possibility is linked to differential effects of PA on neural oscillations. In fact, while PA increases beta power in motor cortices ipsilateral to prismatic deviation 22 , verb retrieval is associated with beta suppression in motor areas 54 .…”

The longitudinal association between externalizing behavior and frontoamygdalar resting‐state functional connectivity in late adolescence and young adulthood

“…Our results of developmental changes in more posterior but not anterior regions are in line with the notion that – compared to regions implicated in sensory and emotional processes – regions involved in cognition follow a more protracted developmental trajectory (Giedd et al, 1999 ; Gogtay et al, 2004 ). However, Van Duijvenvoorde et al ( 2019 ) found no significant longitudinal associations between age and amygdala–ACC functional connectivity, and in a small cross‐sectional study ( N = 58), amygdala–ACC functional connectivity has been suggested to increase over adolescence and young adulthood for more ventral regions of the ACC only (Gabard‐Durnam et al, 2014 ). Thus, the current literature on developmental trajectories of amygdala–ACC functional connectivity shows mixed results and warrants further examination.…”