Neuroanatomical substrates of action perception and understanding: an anatomic likelihood estimation meta-analysis of lesion-symptom mapping studies in brain injured patients

Abstract

Several neurophysiologic and neuroimaging studies suggested that motor and perceptual systems are tightly linked along a continuum rather than providing segregated mechanisms supporting different functions. Using correlational approaches, these studies demonstrated that action observation activates not only visual but also motor brain regions. On the other hand, brain stimulation and brain lesion evidence allows tackling the critical question of whether our action representations are necessary to perceive and understand others' actions. In particular, recent neuropsychological studies have shown that patients with temporal, parietal, and frontal lesions exhibit a number of possible deficits in the visual perception and the understanding of others' actions. The specific anatomical substrates of such neuropsychological deficits however, are still a matter of debate. Here we review the existing literature on this issue and perform an anatomic likelihood estimation meta-analysis of studies using lesion-symptom mapping methods on the causal relation between brain lesions and non-linguistic action perception and understanding deficits. The meta-analysis encompassed data from 361 patients tested in 11 studies and identified regions in the inferior frontal cortex, the inferior parietal cortex and the middle/superior temporal cortex, whose damage is consistently associated with poor performance in action perception and understanding tasks across studies. Interestingly, these areas correspond to the three nodes of the action observation network that are strongly activated in response to visual action perception in neuroimaging research and that have been targeted in previous brain stimulation studies. Thus, brain lesion mapping research provides converging causal evidence that premotor, parietal and temporal regions play a crucial role in action recognition and understanding.

Keywords: action perception; action simulation; action understanding; activation likelihood estimation (ALE) meta-analysis; brain lesion; mirror neurons; voxel-lesion-symptom mapping.

FIGURE 1

Maps of the clusters with significant association between brain lesions and action perception, and understanding disorders overlaid on axial slices (A) or 3D rendering (B) of the Montreal Neurological Institute (MNI) template. Left hemisphere is on the left, and right hemisphere is on the right. Color scale indicates AnLE value range. IFG, inferior frontal gyrus; IPS, intraparietal sulcus; MTG, middle temporal gryus. Note that deeper regions are projected onto the surface of the template to better highlight the extension of the cluster.