Double dissociation of the roles of the left and right prefrontal cortices in anticipatory regulation of action

Abstract

Recent actions can benefit or disrupt our current actions and the prefrontal cortex (PFC) is thought to play a major role in the regulation of these actions before they occur. The left PFC has been associated with overcoming interference from past events in the context of language production and working memory. The right PFC, and especially the right IFG, has been associated with preparatory inhibition processes. But damage to the right PFC has also been associated with impairment in sustaining actions in motor intentional disorders. Moreover, bilateral dorsolateral PFC has been associated with the ability to maintain task-sets, and improve the performance of current actions based on previous experience. However, potential hemispheric asymmetries in anticipatory regulation of action have not yet been delineated. In the present study, patients with left (n=7) vs. right (n=6) PFC damage due to stroke and 14 aged- and education-matched controls performed a picture naming and a verbal Simon task (participants had to say “right” or “left” depending on the color of the picture while ignoring its position). In both tasks, performance depended on the nature of the preceding trial, but in different ways. In the naming task, performance decreased if previous pictures were from the same rather than from different semantic categories (i.e., semantic interference effect). In the Simon task, performance was better for both compatible (i.e., response matching the position of the stimulus) and incompatible trials when preceded by a trial of the same compatibility (i.e. Gratton effect) relative to sequential trials of different compatibility. Left PFC patients were selectively impaired in picture naming; they had an increased semantic interference effect compared to both right PFC patients and aged-matched controls. Conversely, right PFC patients were selectively impaired in the Simon task compared to controls or left PFC patients; they showed no benefit when sequential trials were compatible (cC vs. iC trials) or a decreased Gratton effect. These results provide evidence for a double dissociation between left and right PFC in the anticipatory regulation of action. Our results are in agreement with a preponderant role of the left PFC in overcoming proactive interference from competing memory representations and provide evidence that the right PFC, plays a role in sustaining goal-directed actions consistent with clinical data in right PFC patients with motor intentional disorders.

Specifying the role of the left prefrontal cortex in word selection

“…This paradigm has rarely been studied in older controls and we wanted to examine whether the results were similar to young controls. In addition, we tested whether the left PFC patients tested in this study showed a larger semantic interference effect in the blocked cyclic picture-naming paradigm, using a subset of the data published in Ries et al (2014). As shown on a larger group of patients, we predicted the subset of 6 left PFC patients tested here to show a larger semantic interference effect than age-matched controls in this paradigm involving within block item repetition.…”

“…As explained in Ries et al (2014), in the blocking naming paradigm the first presentation tends to show, if anything, a semantic facilitation effect as a consequence of semantic priming between related items in homogenous blocks (e.g., Abdel-Rahman & Melinger, 2007; Navarrete et al, 2012; see for further discussion on semantic facilitation effects in the blocking paradigm, Navarrete et al, 2014). We tested for fixed effects of Group (2 levels: age-matched controls, and left PFC patients) as a between-subject factor and Semantic Context (homogeneous vs. heterogeneous), Repetition (from 2 to 6), and stimulus position (i.e., left or right of the fixation cross) as within-subject factors, and interactions between Semantic Context, Repetition, and Group.…”

“…The aged-matched control and the patient groups did not differ statistically in terms of age (estimated mean of the difference between groups = 7 years; 95% HDI (highest density interval) =(−7.07, 19.0) 1 ) and age of education (estimated mean of the difference between groups = 1 year; 95% HDI (−4.21, 2.33)), and received remuneration for their participation in the experiment. The age-and-education-matched control group in the blocked-cyclic picture-naming paradigm was the same as the one described in Ries et al (2014). It contained 14 participants (8 females; age: median = 68 years old, IQR = 62–71; years of education: median = 16 years, IQR = 16–18).…”

“…We then turn to the blocked cyclic picture naming paradigm which is also described in Ries et al (2014).…”

“…These have often reported an involvement of the left PFC, and in particular of the LIFG. More specifically, neuropsychological studies have shown that left PFC patients show a larger semantic interference effect than controls (Schnur et al, 2006) and right PFC patients (Ries, Greenhouse, Dronkers, Haaland, & Knight, 2014). In addition, BOLD signal in the LIFG but also in left temporal regions increases in semantically-homogeneous compared to semantically heterogeneous blocks (Hocking et al, 2009; Schnur et al, 2009).…”