No abstract

How neural specificity for distinct conceptual knowledge categories arises is central for understanding the organization of semantic memory in the human brain. Although there is a large body of research on the neural processing of distinct object categories, the organization of action categories remains largely unknown. In particular, it is unknown whether different action categories follow a specific topographical organization on the cortical surface analogously to the category-specific organization of object knowledge. Here, we tested whether the neural representation of action knowledge is organized in terms of nonsocial versus social and object-unrelated versus object-related actions (sociality and transitivity, respectively, hereafter). We hypothesized a major distinction of sociality and transitivity along dorsal and ventral lateral occipitotemporal cortex (LOTC), respectively. Using fMRI-based multivoxel pattern analysis, we identified neural representations of action information associated with sociality and transitivity in bilateral LOTC. Representational similarity analysis revealed a dissociation between dorsal and ventral LOTC. We found that action representations in dorsal LOTC are segregated along features of sociality, whereas action representations in ventral LOTC are segregated along features of transitivity. In addition, representations of sociality and transitivity features were found more anteriorly in LOTC than representations of specific subtypes of actions, suggesting a posterior-anterior gradient from concrete to abstract action features. These findings elucidate how the neural representations of perceptually and conceptually diverse actions are organized in distinct subsystems in the LOTC.

Brain regions that mediate action understanding must contain representations that are action specific and at the same time tolerate a wide range of perceptual variance. Whereas progress has been made in understanding such generalization mechanisms in the object domain, the neural mechanisms to conceptualize actions remain unknown. In particular, there is ongoing dissent between motor-centric and cognitive accounts whether premotor cortex or brain regions in closer relation to perceptual systems, i.e., lateral occipitotemporal cortex, contain neural populations with such mapping properties. To date, it is unclear to which degree action-specific representations in these brain regions generalize from concrete action instantiations to abstract action concepts. However, such information would be crucial to differentiate between motor and cognitive theories. Using ROI-based and searchlight-based fMRI multivoxel pattern decoding, we sought brain regions in human cortex that manage the balancing act between specificity and generality. We investigated a concrete level that distinguishes actions based on perceptual features (e.g., opening vs closing a specific bottle), an intermediate level that generalizes across movement kinematics and specific objects involved in the action (e.g., opening different bottles with cork or screw cap), and an abstract level that additionally generalizes across object category (e.g., opening bottles or boxes). We demonstrate that the inferior parietal and occipitotemporal cortex code actions at abstract levels whereas the premotor cortex codes actions at the concrete level only. Hence, occipitotemporal, but not premotor, regions fulfill the necessary criteria for action understanding. This result is compatible with cognitive theories but strongly undermines motor theories of action understanding.

Neurons in macaque ventral premotor cortex and inferior parietal lobe discharge during both the observation and the execution of motor acts. It has been claimed that these so-called mirror neurons form the basis of action understanding by matching the visual input with the corresponding motor program (direct matching). Functional magnetic resonance imaging (fMRI) adaptation can be used to test the direct matching account of action recognition by determining whether putative mirror neurons show adaptation for repeated motor acts independently of whether they are observed or executed. An unambiguous test of the hypothesis requires that the motor acts be meaningless to ensure that any adaptation effect is directly because of movement recognition/motor execution and not contextually determined inferences. We found adaptation for motor acts that were repeatedly observed or repeatedly executed. We also found adaptation for motor acts that were first observed and then executed, as would be expected if a previously seen act primed the subsequent execution of that act. Crucially, we found no signs of adaptation for motor acts that were first executed and then observed. Failure to find cross-modal adaptation for executed and observed motor acts is not compatible with the core assumption of mirror neuron theory, which holds that action recognition and understanding are based on motor simulation. embodied cognition ͉ motor action recognition ͉ motor theory of action recognition