In both monkeys and humans, the observation of actions performed by others activates cortical motor areas. An unresolved question concerns the pathways through which motor areas receive visual information describing motor acts. Using functional magnetic resonance imaging (fMRI), we mapped the macaque brain regions activated during the observation of grasping actions, focusing on the superior temporal sulcus region (STS) and the posterior parietal lobe. Monkeys viewed either videos with only the grasping hand visible or videos with the whole actor visible. Observation of both types of grasping videos activated elongated regions in the depths of both lower and upper banks of STS, as well as parietal areas PFG and anterior intraparietal (AIP). The correlation of fMRI data with connectional data showed that visual action information, encoded in the STS, is forwarded to ventral premotor cortex (F5) along two distinct functional routes. One route connects the upper bank of the STS with area PFG, which projects, in turn, to the premotor area F5c. The other connects the anterior part of the lower bank of the STS with premotor areas F5a/p via AIP. Whereas the first functional route emphasizes the agent and may relay visual information to the parieto-frontal mirror circuit involved in understanding the agent's intentions, the second route emphasizes the object of the action and may aid in understanding motor acts with respect to their immediate goal.

Research in recent decades has suggested the existence of a dedicated brain network devoted to the organization and execution of grasping, one of the most important and skilled movements of primates. Grasping an object requires the transformation of intrinsic object properties such as size, orientation, and shape into an appropriate motor scheme shaping the hand. Although electrophysiological recordings in the monkey model have proven invaluable for gaining insights into the neuronal substrate underlying this complex behavior, knowledge concerning the existence and organization of a similar system in the human brain is derived mainly from imaging studies. Here, we present for the first time functional magnetic resonance imaging (fMRI) of brain activity while macaque monkeys performed reaching and grasping movements in a 3 tesla MR scanner. Grasping in the dark (compared with reaching) yielded significant activations in anterior intraparietal area and ventral premotor area F5, in addition to area PFG in the rostral inferior parietal lobule, somatosensory areas (SI, SII, area 5), and the hand field of F1. Whole-brain macaque fMRI motor studies will be instrumental in establishing possible homologies concerning grasping organization in the human and monkey brains, bridging the gap between human imaging and monkey electrophysiology.

Prehension movements typically include a reaching phase, guiding the hand toward the object, and a grip phase, shaping the hand around it. The dominant view posits that these components rely upon largely independent parieto-frontal circuits: a dorso-medial circuit involved in reaching and a dorso-lateral circuit involved in grasping. However, mounting evidence suggests a more complex arrangement, with dorso-medial areas contributing to both reaching and grasping. To investigate the role of the dorso-medial reaching circuit in grasping, we trained monkeys to reach-and-grasp different objects in the dark and determined if hand configurations could be decoded from functional magnetic resonance imaging (MRI) responses obtained from the reaching and grasping circuits. Indicative of their established role in grasping, object-specific grasp decoding was found in anterior intraparietal (AIP) area, inferior parietal lobule area PFG and ventral premotor region F5 of the lateral grasping circuit, and primary motor cortex. Importantly, the medial reaching circuit also conveyed robust grasp-specific information, as evidenced by significant decoding in parietal reach regions (particular V6A) and dorsal premotor region F2. These data support the proposed role of dorso-medial “reach” regions in controlling aspects of grasping and demonstrate the value of complementing univariate with more sensitive multivariate analyses of functional MRI (fMRI) data in uncovering information coding in the brain.

Neurophysiological data obtained in primates suggests that merely observing others' actions can modulate activity in the observer's motor cortices. In humans, it has been suggested that these multimodal vicarious responses extend well beyond the motor cortices, including somatosensory and insular brain regions, which seem to yield vicarious responses when witnessing others' actions, sensations, or emotions (Gazzola and Keysers, 2009). Despite the wealth of data with respect to shared action responses in the monkey motor system, whether the somatosensory and insular cortices also yield vicarious responses during observation of touch remains largely unknown. Using independent tactile and motor fMRI localizers, we first mapped the hand representations of two male monkeys' primary (SI) and secondary (SII) somatosensory cortices. In two subsequent visual experiments, we examined fMRI brain responses to (1) observing a conspecific's hand being touched or (2) observing a human hand grasping or mere touching an object or another human hand. Whereas functionally defined “tactile SI” and “tactile SII” showed little involvement in representing observed touch, vicarious responses for touch were found in parietal area PFG, consistent with recent observations in humans (Chan and Baker, 2015). Interestingly, a more anterior portion of SII, and posterior insular cortex, both of which responded when monkeys performed active grasping movements, also yielded visual responses during different instances of touch observation.SIGNIFICANCE STATEMENTCommon coding of one's own and others' actions, sensations, and emotions seems to be widespread in the brain. Although it is currently unclear to what extent human somatosensory cortices yield vicarious responses when observing touch, even less is known about the presence of similar vicarious responses in monkey somatosensory cortex. We therefore localized monkey somatosensory hand representations using fMRI and investigated whether these regions yield vicarious responses while observing various instances of touch. Whereas “tactile SI and SII” did not elicit responses during touch observation, a more anterior portion of SII, in addition to area PFG and posterior insular cortex, all of which responded during monkeys' own grasping movements, yielded vicarious responses during observed touch.

We used contrast-agent enhanced functional magnetic resonance imaging (fMRI) in the alert monkey to map the cortical regions involved in the extraction of 3D shape from the monocular static cues, texture and shading. As in the parallel human imaging study [1], we contrasted the 3D condition to several 2D control conditions. The extraction of 3D shape from texture (3D SfT) involves both ventral and parietal regions, in addition to early visual areas. Strongest activation was observed in CIP, with decreasing strength towards the anterior part of the intraparietal sulcus (IPS). In the ventral stream 3D SfT sensitivity was observed in a ventral portion of TEO. The extraction of 3D shape from shading (3D SfS) involved predominantly ventral regions, such as V4 and a dorsal potion of TEO. These results are similar to those obtained earlier in human subjects and indicate that the extraction of 3D shape from texture is performed in both ventral and dorsal regions for both species, as are the motion and disparity cues, whereas shading is mainly processed in the ventral stream.