The inferior frontal gyrus and inferior parietal lobe have been characterized as human homologues of the monkey “mirror neuron” system, critical for both action production (AP) and action recognition (AR). However, data from brain lesion patients with selective impairment on only one of these tasks provide evidence of neural and cognitive dissociations. We sought to clarify the relationship between AP and AR, and their critical neural substrates, by directly comparing performance of 131 chronic left-hemisphere stroke patients on both tasks—to our knowledge, the largest lesion-based experimental investigation of action cognition to date. Using voxel-based lesion-symptom mapping, we found that lesions to primary motor and somatosensory cortices and inferior parietal lobule were associated with disproportionately impaired performance on AP, whereas lesions to lateral temporo-occipital cortex were associated with a relatively rare pattern of disproportionately impaired performance on AR. In contrast, damage to posterior middle temporal gyrus was associated with impairment on both AP and AR. The distinction between lateral temporo-occipital cortex, critical for recognition, and posterior middle temporal gyrus, important for both tasks, suggests a rough gradient from modality-specific to abstract representations in posterior temporal cortex, the first lesion-based evidence for this phenomenon. Overall, the results of this large patient study help to bring closure to a long-standing debate by showing that tool-related AP and AR critically depend on both common and distinct left hemisphere neural substrates, most of which are external to putative human mirror regions.

Many recent neuroimaging studies have investigated the representation of semantic memory for actions in the brain. We used activation likelihood estimation (ALE) meta-analyses to answer two outstanding questions about the neural basis of action concepts. First, on an “embodied” view of semantic memory, evidence to date is unclear regarding whether visual motion or motor systems are more consistently engaged by action concepts. Second, few studies have directly investigated the possibility that action concepts accessed verbally or nonverbally recruit different areas of the brain. Because our meta-analyses did not include studies requiring the perception of dynamic depictions of actions or action execution, we were able to determine whether conceptual processing alone recruits visual motion and motor systems. Significant concordance in brain regions within or adjacent to visual motion areas emerged in all meta-analyses. By contrast, we did not observe significant concordance in motor or premotor cortices in any analysis. Neural differences between action images and action verbs followed a gradient of abstraction among representations derived from visual motion information in the left lateral temporal and occipital cortex. The consistent involvement of visual motion but not motor brain regions in representing action concepts may reflect differences in the variability of experience across individuals with perceiving versus performing actions.