Frontal and parietal cortex contributions to action modification

Abstract

Successful achievement of task goals depends critically on the ability to adjust ongoing actions in response to environmental changes. The neural substrates underlying action modification have been a topic of great controversy: both, posterior parietal cortex and frontal regions, particularly prefrontal cortex have been previously identified as crucial in this regard, with most studies arguing in favor of one or the other. We aimed to address this controversy and understand whether frontal and parietal regions might play distinct roles during action modification. We tested ipsilesional arm performance of 27 stroke patients with focal lesions to frontal or parietal regions of the left or right cerebral hemisphere, and left or right arm performance of 18 healthy subjects on the classic double-step task in which a target is unpredictably displaced to a new location, requiring modification of the ongoing action. Only right hemisphere frontal lesions adversely impacted the timing of initiation of the modified response, while only left hemisphere parietal lesions impaired the accuracy of the modified action. Patients with right frontal lesions tended to complete the ongoing action to the initially displayed baseline target and initiated the new movement after a significant delay. In contrast, patients with left parietal damage did not accurately reach the new target location, but compared to the other groups, initiated the new action during an earlier phase of motion, before their baseline action was complete. Our findings thus suggest distinct, hemisphere specific contributions of frontal and parietal regions to action modification, and bring together, for the first time, disparate sets of prior findings about its underlying neural substrates.

Introduction

The ability to appropriately modify our actions whenever environmental changes so demand is crucial for successfully accomplishing task goals. Here we sought to delineate the contributions of posterior parietal and frontal regions to action modification; both these regions have previously been independently and exclusively implicated in action modification, resulting in great controversy about its underlying neural substrates.

Several studies have strongly advocated a principal role for posterior parietal cortex (PPC) in the adjustment of ongoing actions. The seminal study of Desmurget et al. (1999) first demonstrated that transcranial magnetic stimulation (TMS) to left PPC disrupted modifications of ongoing right arm movements following changes in the location of a reaching target (“double-step” task). Modification of ongoing left arm actions was not disrupted after left parietal TMS, leading the authors to suggest that parietal contributions to action modification are strictly contralateral. Such effects of left parietal stimulation on right arm adjustments have since been corroborated by other studies (Glover et al., 2005, Tunik et al., 2005). Further, imaging studies (Desmurget et al., 2001, Diedrichsen et al., 2005, Reichenbach et al., 2011) have found PPC activation during double-step tasks performed with one arm, but these studies have reported that such activation is often bilateral in nature. Studies in patients have also demonstrated deficient action modification following PPC lesions, but these studies have relied on cases with bilateral parietal damage (Grea et al., 2002, Pisella et al., 2000). Thus, while these studies have not been able to clearly delineate whether parietal regions in a single or both hemispheres are crucial, they have all clearly highlighted parietal involvement during action modification.

Controversy emerges however from the findings of studies employing simpler tasks to probe for cognitive processes contributing to action modification (e.g., pressing a different button when the cue color is unexpectedly changed). These studies have repeatedly emphasized frontal regions, as the critical underlying neural substrate. Additionally, these studies have suggested that frontal contribution appears to be hemispherically asymmetric, with a predominant role for frontal regions of the right hemisphere during action modification. These imaging (Aron et al., 2007, Mars et al., 2007), TMS (Buch et al., 2010, Neubert et al., 2010) and patient studies (Greenhouse, Gould, Houser, & Aron, 2013) have identified a crucial role for the right inferior frontal gyrus, as well as other frontal cortical and subcortical regions in a distributed right hemisphere based action “reprogramming” network. Interestingly, Mars et al. (2007) reported that along with activation in right frontal regions, left parietal regions were also active when an ongoing action had to be modified. Crucially however, unlike the right frontal activation that emerged specifically during action modification, left parietal activation was evident also when any stable action had to be made, suggesting that these two regions might play distinct roles when the need to correct an ongoing action emerged.

Our recent results (Schaefer, Mutha, Haaland, & Sainburg, 2012) examining the impact of distributed left and right hemisphere damage on the ability to modify an ongoing action are in line with this suggestion. We found that both left and right hemisphere damage disrupted the ability to correct an ongoing movement in a double-step task when it was performed with the ipsilesional arm. However, the nature of the deficit was different depending on the hemisphere of damage, suggesting hemispherically specific contributions to this process. While left hemisphere damage disrupted the coordination of the corrective response that correlated with a disruption in accuracy, right hemisphere damage disrupted the timing and accuracy of the correction while sparing the coordination of the corrective action. Here we wished to build upon these findings and probe specifically whether frontal and parietal contributions to action modification are distinct and hemispherically lateralized. We thus aimed to address the controversial findings in the literature (cited above) and understand whether the left parietal and right frontal regions play different but complementary roles during action modification. Based on these studies and our own recent results, we predicted distinct deficits in the ipsilesional arm during the double-step task after focal left parietal and right frontal damage.