Major theories for explaining the organization of semantic memory in the human brain are premised on the often-observed dichotomous dissociation between living and nonliving objects. Evidence from neuroimaging has been interpreted to suggest that this distinction is reflected in the functional topography of the ventral vision pathway as lateral-to-medial activation gradients. Recently, we observed that similar activation gradients also reflect differences among living stimuli consistent with the semantic dimension of graded animacy. Here, we address whether the salient dichotomous distinction between living and nonliving objects is actually reflected in observable measured brain activity or whether previous observations of a dichotomous dissociation were the illusory result of stimulus sampling biases. Using fMRI, we measured neural responses while participants viewed 10 animal species with high to low animacy and two inanimate categories. Representational similarity analysis of the activity in ventral vision cortex revealed a main axis of variation with high-animacy species maximally different from artifacts and with the least animate species closest to artifacts. Although the associated functional topography mirrored activation gradients observed for animate–inanimate contrasts, we found no evidence for a dichotomous dissociation. We conclude that a central organizing principle of human object vision corresponds to the graded psychological property of animacy with no clear distinction between living and nonliving stimuli. The lack of evidence for a dichotomous dissociation in the measured brain activity challenges theories based on this premise.

Facial expressions and hand gestures are utilized in nonverbal communication to convey socially relevant information. One key process that mediates nonverbal communication is simulation. The mirror neuron system (MNS), which maps observed actions onto the motor representations used when producing those actions, likely plays a role in simulation. Previous neuroimaging experiments have identified a putative human MNS that includes the inferior parietal lobule (IPL) and the frontal operculum. Although understanding nonverbal communication presumably involves the MNS, it is unknown whether these two forms of nonverbal social communication have distinct representations within that system. Here we report the results of a functional magnetic resonance imaging experiment in which participants viewed, imitated, and produced facial expressions and social hand gestures. The observation and execution of facial expressions and social hand gestures activated the MNS, but the magnitude of response differed. Activation in the IPL was greater for social hand gestures, whereas activation in the frontal operculum was greater for viewing facial expressions. The locations of neural activity evoked by viewing facial expressions and social hand gestures in the frontal operculum were significantly different. These data argue that there are distinct representations of different types of social nonverbal communication in the MNS.

We compared two tasks that are widely used in research on mentalizing—false belief stories and animations of rigid geometric shapes that depict social interactions—to investigate whether the neural systems that mediate the representation of others' mental states are consistent across these tasks. Whereas false belief stories activated primarily the anterior paracingulate cortex (APC), the posterior cingulate cortex/precuneus (PCC/PC), and the temporo-parietal junction (TPJ)—components of the distributed neural system for theory of mind (ToM)—the social animations activated an extensive region along nearly the full extent of the superior temporal sulcus, including a locus in the posterior superior temporal sulcus (pSTS), as well as the frontal operculum and inferior parietal lobule (IPL)—components of the distributed neural system for action understanding—and the fusiform gyrus. These results suggest that the representation of covert mental states that may predict behavior and the representation of intentions that are implied by perceived actions involve distinct neural systems. These results show that the TPJ and the pSTS play dissociable roles in mentalizing and are parts of different distributed neural systems. Because the social animations do not depict articulated body movements, these results also highlight that the perception of the kinematics of actions is not necessary to activate the mirror neuron system, suggesting that this system plays a general role in the representation of intentions and goals of actions. Furthermore, these results suggest that the fusiform gyrus plays a general role in the representation of visual stimuli that signify agency, independent of visual form.

Deciding whether an unfamiliar person is trustworthy is one of the most important decisions in social environments. We used functional magnetic resonance imaging to show that the amygdala is involved in implicit evaluations of trustworthiness of faces, consistent with prior findings. The amygdala response increased as perceived trustworthiness decreased in a task that did not demand person evaluation. More importantly, we tested whether this response is due to an individual's idiosyncratic perception or to face properties that are perceived as untrustworthy across individuals. The amygdala response was better predicted by consensus ratings of trustworthiness than by an individual's own judgments. Individual judgments accounted for little residual variance in the amygdala after controlling for the shared variance with consensus ratings. These findings suggest that the amygdala automatically categorizes faces according to face properties commonly perceived to signal untrustworthiness.

Object and face representations in ventral temporal (VT) cortex were investigated by combining object confusability data from a computational model of object classification with neural response confusability data from a functional neuroimaging experiment. A pattern-based classification algorithm learned to categorize individual brain maps according to the object category being viewed by the subject. An identical algorithm learned to classify an image-based, view-dependent representation of the stimuli. High correlations were found between the confusability of object categories and the confusability of brain activity maps. This occurred even with the inclusion of multiple views of objects, and when the object classification model was tested with high spatial frequency “line drawings” of the stimuli. Consistent with a distributed representation of objects in VT cortex, the data indicate that object categories with shared image-based attributes have shared neural structure.

We used fMRI to study the organization of brain responses to different types of complex visual motion. In a rapid eventrelated design, subjects viewed video clips of humans performing different whole-body motions, video clips of manmade manipulable objects (tools) moving with their characteristic natural motion, point-light displays of human whole-body motion, and point-light displays of manipulable objects. The lateral temporal cortex showed strong responses to both moving videos and moving point-light displays, supporting the hypothesis that the lateral temporal cortex is the cortical locus for processing complex visual motion. Within the lateral temporal cortex, we observed segregated responses to different types of motion. The superior temporal sulcus (STS) responded strongly to human videos and human point-light displays, while the middle temporal gyrus (MTG) and the inferior temporal sulcus responded strongly to tool videos and tool point-light displays. In the ventral temporal cortex, the lateral fusiform responded more to human videos than to any other stimulus category while the medial fusiform preferred tool videos. The relatively weak responses observed to point-light displays in the ventral temporal cortex suggests that form, color, and texture (present in video but not point-light displays) are the main contributors to ventral temporal activity. In contrast, in the lateral temporal cortex, the MTG responded as strongly to point-light displays as to videos, suggesting that motion is the key determinant of response in the MTG. Whereas the STS responded strongly to point-light displays, it showed an even larger response to video displays, suggesting that the STS integrates form, color, and motion information.

Recently, we identified, using fMRI, three bilateral regions in the ventral temporal cortex that responded preferentially to faces, houses, and chairs [Ishai, A., Ungerleider, L. G., Martin, A., Schouten, J. L., & Haxby, J. Y. (1999). Distributed representation of objects in the human ventral visual pathway. Proceedings of the National Academy of Sciences, U.S.A., 96 , 9379-9384]. Here, we report differential patterns of activation, similar to those seen in the ventral temporal cortex, in bilateral regions of the ventral occipital cortex. We also found category-related responses in the dorsal occipital cortex and in the superior temporal sulcus. Moreover, rather than activating discrete, segregated areas, each category was associated with its own differential pattern of response across a broad expanse of cortex. The distributed patterns of response were similar across tasks (passive viewing, delayed matching) and presentation formats (photographs, line drawings). We propose that the representation of objects in the ventral visual pathway, including both occipital and temporal regions, is not restricted to small, highly selective patches of cortex but, instead, is a distributed representation of information about object form. Within this distributed system, the representation of faces appears to be less extensive as compared to the representations of nonface objects.

This study examines important developmental differences in patterns of activation in the prefrontal cortex during performance of a Go-No-Go paradigm using functional magnetic resonance imaging (fMRI). Eighteen subjects (9 children and 9 adults) were scanned using gradient echo, echo planar imaging during performance of a response inhibition task. The results suggest four general findings. First, the location of activation in the prefrontal cortex was not different between children and adults, which is similar to our earlier pediatric fMRI results of prefrontal activation during a working memory task (Casey et al., 1995). Second, the volume of activation was significantly greater for children relative to adults. These differences in volume of activation were observed predominantly in the dorsal and lateral prefrontal cortices. Third, although inhibitory processes have typically been associated with more ventral or orbital frontal regions, the current study revealed activation that was distributed across both dorsolateral and orbitofrontal cortices. Finally, consistent with animal and human lesion studies, activity in orbital frontal and anterior cingulate cortices correlated with behavioral performance (i.e., number of false alarms). These results further demonstrate the utility of this methodology in studying pediatric populations.

Primate extrastriate visual cortex is organized into an occipitotemporal pathway for object vision and an occipitoparietal pathway for spatial vision. Correlations between normalized regional cerebral blood flow values (regional divided by global flows), obtained using H 2 15 O and positron emission tomography, were used to examine functional associations among posterior brain regions for these two pathways in 17 young men during performance of a face matching task and a dot-location matching task. During face matching, there was a significant correlation in the right hemisphere between an extrastriate occipital region that was equally activated during both the face matching and dot-location matching tasks and a region in inferior occipitotemporal cortex that was activated more during the face matching task. The corresponding correlation in the left hemisphere was not significantly different from zero. Significant intrahemispheric correlations among posterior regions were observed more often for the right than for the left hemisphere. During dot-location matching, many significant correlations were found among posterior regions in both hemispheres, but significant correlations between specific regions in occipital and parietal cortex shown to be reliably activated during this spatial vision test were found only in the right cerebral hemisphere. These results suggest that (1) correlational analysis of normalized rCBF can detect functional interactions between components of proposed brain circuits, and (2) face and dot-location matching depend primarily on functional interactions between posterior cortical areas in the right cerebral hemisphere. At the same time, left hemisphere cerebral processing may contribute more to dot-location matching than to face matching.

We previously reported selective activation of regional cerebral blood flow (rCBF) in occipitotemporal cortex during a face matching task (object vision) and activation in superior parietal cortex during a dot-location matching task (spatial vision) in young subjects, The purpose of the present study was to determine the effects of aging on these extrastriate visual processing systems. Eleven young (mean age 27 ± 4 years) and nine old (mean age 72 ± 7 years) male subjects were studied. Positron emission tomographic scans were performed using a Scanditronix PC1024–7B tomograph and H 2 15 O to measure rCBF. To locate brain areas that were activated by the visual tasks, pixel-by-pixel difference images were computed between images from a control task and images from the face and dot-location matching tasks. Both young and old subjects showed rCBF activation during face matching primarily in occipitotemporal cortex, and activation of superior parietal cortex during dot-location matching. Statistical comparisons of these activations showed that the old subjects had more activation of occipitotemporal cortex during the spatial task and more activation of superior parietal cortex during the object task than did the young subjects. These results show less functional separation of the dorsal and ventral visual pathways in older subjects, and may reflect an age-related reduction in the processing efficiency of these visual cortical areas.