Superior Temporal Sulcus Region Research Articles

Dissociable Roles of the Superior Temporal Sulcus and the Intraparietal Sulcus in Joint Attention: A Functional Magnetic Resonance Imaging Study

Abstract Previous imaging work has shown that the superior temporal sulcus (STS) region and the intraparietal sulcus (IPS) are specifically activated during the passive observation of shifts in eye gaze [Pelphrey, K. A., Singerman, J. D., Allison, T., & McCarthy, G. Brain activation evoked by perception of gaze shifts: The influence of context. Neuropsychologia, 41, 156-170, 2003; Hoffman, E. A., & Haxby, J. V. Distinct representations of eye gaze and identity in the distributed human neural system for face perception. Nature Neuroscience, 3, 80-84, 2000; Puce, A., Allison, T., Bentin, S., Gore, J. C., & McCarthy, G. Temporal cortex activation in humans viewing eye and mouth movements. Journal of Neuroscience, 18, 2188-2199, 1998; Wicker, B., Michel, F., Henaff, M. A., & Decety, J. Brain regions involved in the perception of gaze: A PET study. Neuroimage, 8, 221-227, 1998]. Are the same brain regions also involved in extracting gaze direction in order to establish joint attention? In an event-related functional magnetic resonance imaging experiment, healthy human subjects actively followed the directional cue provided by the eyes of another person toward an object in space or, in the control condition, used a nondirectional symbolic cue to make an eye movement toward an object in space. Our results show that the posterior part of the STS region and the cuneus are specifically involved in extracting and using detailed directional information from the eyes of another person to redirect one's own gaze and establish joint attention. The IPS, on the other hand, seems to be involved in encoding spatial direction and mediating shifts of spatial attention independent of the type of cue that triggers this process.

Dissociable Roles of the Superior Temporal Sulcus and the Intraparietal Sulcus in Joint Attention: A Functional Magnetic Resonance Imaging Study

Abstract Previous imaging work has shown that the superior temporal sulcus (STS) region and the intraparietal sulcus (IPS) are specifically activated during the passive observation of shifts in eye gaze [Pelphrey, K. A., Singerman, J. D., Allison, T., & McCarthy, G. Brain activation evoked by perception of gaze shifts: The influence of context. Neuropsychologia, 41, 156–170, 2003; Hoffman, E. A., & Haxby, J. V. Distinct representations of eye gaze and identity in the distributed human neural system for face perception. Nature Neuroscience, 3, 80–84, 2000; Puce, A., Allison, T., Bentin, S., Gore, J. C., & McCarthy, G. Temporal cortex activation in humans viewing eye and mouth movements. Journal of Neuroscience, 18, 2188–2199, 1998; Wicker, B., Michel, F., Henaff, M. A., & Decety, J. Brain regions involved in the perception of gaze: A PET study. Neuroimage, 8, 221–227, 1998]. Are the same brain regions also involved in extracting gaze direction in order to establish joint attention? In an event-related functional magnetic resonance imaging experiment, healthy human subjects actively followed the directional cue provided by the eyes of another person toward an object in space or, in the control condition, used a nondirectional symbolic cue to make an eye movement toward an object in space. Our results show that the posterior part of the STS region and the cuneus are specifically involved in extracting and using detailed directional information from the eyes of another person to redirect one's own gaze and establish joint attention. The IPS, on the other hand, seems to be involved in encoding spatial direction and mediating shifts of spatial attention independent of the type of cue that triggers this process.

Cognitive control in social situations: A role for the dorsolateral prefrontal cortex

Using functional magnetic resonance imaging (fMRI), we investigated brain activity elicited by a computer-animated child's actions that appeared consistent and inconsistent with a computer-animated adult's instructions. Participants observed a computer-animated adult verbally instructing a computer-animated child to touch one of two objects. The child performed correctly in half of the trials and incorrectly in the other half. We observed significantly greater activity when the child performed incorrectly compared to correctly in regions of the dorsolateral prefrontal cortex (DLPFC) that have been implicated in maintaining our intentions in working memory and implementing cognitive control. However, no such effects were found in regions of the posterior superior temporal sulcus (posterior STS) that have been posited to interpret other people's behavior. These findings extend the role of the DLPFC in cognitive control to evaluating the social outcomes of other people's behavior and provide important new constraints for theories of how the posterior STS contributes to social cognition.

Early Face Processing Specificity: It's in the Eyes!

Unlike most other objects that are processed analytically, faces are processed configurally. This configural processing is reflected early in visual processing following face inversion and contrast reversal, as an increase in the N170 amplitude, a scalp-recorded event-related potential. Here, we show that these face-specific effects are mediated by the eye region. That is, they occurred only when the eyes were present, but not when eyes were removed from the face. The N170 recorded to inverted and negative faces likely reflects the processing of the eyes. We propose a neural model of face processing in which face- and eye-selective neurons situated in the superior temporal sulcus region of the human brain respond differently to the face configuration and to the eyes depending on the face context. This dynamic response modulation accounts for the N170 variations reported in the literature. The eyes may be central to what makes faces so special.

Action-Related Properties Shape Object Representations in the Ventral Stream

The principles driving the organization of the ventral object-processing stream remain unknown. Here, we show that stimulus-specific repetition suppression (RS) in one region of the ventral stream is biased according to motor-relevant properties of objects. Quantitative analysis confirmed that this result was not confounded with similarity in visual shape. A similar pattern of biases in RS according to motor-relevant properties of objects was observed in dorsal stream regions in the left hemisphere. These findings suggest that neural specificity for "tools" in the ventral stream is driven by similarity metrics computed over motor-relevant information represented in dorsal structures. Support for this view is provided by converging results from functional connectivity analyses of the fMRI data and a separate neuropsychological study. More generally, these data suggest that a basic organizing principle giving rise to "category specificity" in the ventral stream may involve similarity metrics computed over information represented elsewhere in the brain.

Common and distinct brain activation to viewing dynamic sequences of face and hand movements

The superior temporal sulcus (STS) and surrounding lateral temporal and inferior parietal cortices are an important part of a network involved in the processing of biological movement. It is unclear whether the STS responds to the movement of different body parts uniformly, or if the response depends on the body part that is moving. Here we examined brain activity to recognizing sequences of face and hand movements as well as radial grating motion, controlling for differences in movement dynamics between stimuli. A region of the right posterior STS (pSTS) showed common activation to both face and hand motion, relative to radial grating motion, with no significant difference between responses to face and hand motion in this region. Distinct responses to face motion relative to hand motion were observed in the right mid-STS, while the right posterior inferior temporal sulcus (pITS) and inferior parietal lobule (IPL) showed greater responses to hand motion relative to face motion. These findings indicate that while there may be distinct processing of different body part motion in lateral temporal and inferior parietal cortices, the response of the pSTS is not body part specific. This region may provide input to other parts of a network involved with processing human actions with a high-level visual description of biological motion.

Perception of dynamic changes in facial affect and identity in autism.

Despite elegant behavioral descriptions of abnormalities for processing emotional facial expressions and biological motion in autism, identification of the neural mechanisms underlying these abnormalities remains a critical and largely unmet challenge. We compared brain activity with dynamic and static facial expressions in participants with and without high-functioning autism using event-related functional magnetic resonance imaging (fMRI) and three classes of face stimuli-emotion morphs (fearful and angry), identity morphs and static images (fearful, angry and neutral). We observed reduced activity in the amygdala (AMY) and fusiform gyrus (FFG) to dynamic emotional expressions in people with autism. There was also a lack of modulation by dynamic compared with static emotional expressions of social brain regions including the AMY, posterior superior temporal sulcus (STS) region and FFG. We observed equivalent emotion and identity morph-evoked activity in participants with and without autism in a region corresponding to the expected location of the more generally motion-sensitive area MT or V5. We conclude that dysfunctions in key components of the human face processing system including the AMY, FFG and posterior STS region are present in individuals with high-functioning autism, and this dysfunction might contribute to the deficits in processing emotional facial expressions.

Separate Coding of Different Gaze Directions in the Superior Temporal Sulcus and Inferior Parietal Lobule

SummaryElectrophysiological recording in the anterior superior temporal sulcus (STS) of monkeys has demonstrated separate cell populations responsive to direct and averted gaze 1, 2. Human functional imaging has demonstrated posterior STS activation in gaze processing, particularly in coding the intentions conveyed by gaze 3, 4, 5, 6, but to date has provided no evidence of dissociable coding of different gaze directions. Because the spatial resolution typical of group-based fMRI studies (∼6–10 mm) exceeds the size of cellular patches sensitive to different facial characteristics (1–4 mm in monkeys), a more sensitive technique may be required. We therefore used fMRI adaptation, which is considered to offer superior resolution [7], to investigate whether the human anterior STS contains representations of different gaze directions, as suggested by non-human primate research. Subjects viewed probe faces gazing left, directly ahead, or right. Adapting to leftward gaze produced a reduction in BOLD response to left relative to right (and direct) gaze probes in the anterior STS and inferior parietal cortex; rightward gaze adaptation produced a corresponding reduction to right gaze probes. Consistent with these findings, averted gaze in the adapted direction was misidentified as direct. Our study provides the first human evidence of dissociable neural systems for left and right gaze.

School-aged children exhibit domain-specific responses to biological motion

Prior studies have implicated the superior temporal sulcus region for processing various types of biological motion in children and adults. However, no previous research in children compared this activity to that involved in coherent, meaningful, non-biological motion perception to show specificity for biological motion processing. In this study, we used functional magnetic resonance imaging to explore which brain regions were specific for biological motion in 7- to 10-year-old children. We compared brain activity in response to biological motion by a biological figure (a walking human); biological motion by a non-biological figure (a walking robot); disorganized, non-biological motion by a disjointed mechanical figure; and organized, non-biological motion by a grandfather clock. We identified a network of brain regions that had a greater response evoked by biological than by non-biological motion, including the superior temporal sulcus and mirror neuron regions. Additionally, we found a developmental change suggesting increasing specificity for biological motion with age in the superior temporal sulcus region. We discuss these results in the context of research and theory that has emphasized the important role of biological motion perception in the development of theory-of-mind abilities.

Brain Mechanisms for Interpreting the Actions of Others From Biological-Motion Cues

Humans are an intensely social species. Our social abilities depend upon specialized brain systems for rapidly recognizing the faces of others, for interpreting the actions of others through an analysis of biological-motion cues, and for determining the emotional states of others via inspection of facial expression. Recent work has implicated the superior temporal sulcus (STS) region as an important component of the social brain. Functional neuroimaging studies have provided clues about how this region is involved in the visual analysis and interpretation of other people's actions. STS activity is modulated by the context within which the actions of biological entities are observed. Such a contextual influence is consistent with a broader tradition within social psychology emphasizing the powerful influences of situational and contextual factors on behavior and perception. The STS region also shows promise as a region of importance in the investigation of both typical and impaired social-cognitive development. Future work should aim to inform us better of the development of interrelationships between the STS region and other regions of the social brain, including the amygdala and the fusiform gyrus.

A deficit in discriminating gaze direction in a case with right superior temporal gyrus lesion

The superior temporal sulcus (STS) region is well recognized as being heavily involved in detecting and discriminating gaze. Lesions confined to this area are quite rare in humans, and so the research has mainly depended on animal studies and functional neuroimaging in normal human subjects. We report one such rare case, a 54-year-old Japanese female with a possible congenital s anomaly who, after a cerebral hemorrhage, demonstrated a lesion almost completely confined to the entire right superior temporal gyrus (STG). In the subacute phase, the patient showed evidence of left hemispatial neglect, from which she gradually recovered. In the chronic phase, she showed a puzzling difficulty in obtaining eye-contact. We have conducted, in conjunction with conventional neuropsychological evaluations, experimental assessment of her ability in gaze cognition. Her performance on neuropsychological testing demonstrated no compromise in intellect, memory, or language skills, and a close-to-full recovery from neglect. On gaze cognition experiments, she was repeatedly shown to perceive left gaze as straight, and to a lesser degree, straight gaze as right. We suggest that the function of the STG in detecting gaze, together with the directional information it receives from earlier visual areas, may be associated, when damaged, with this deficit in detecting contra-directional gaze. We have demonstrated for the first time that a single circumscribed lesion to the STG results in both gaze processing deficit and concurrent aberrant gaze behavior of the victim herself, implicating a mechanism within the STG as an interface between gaze of others and gaze of self.

Differential Characteristics of Face Neuron Responses Within the Anterior Superior Temporal Sulcus of Macaques

The anterior superior temporal sulcus (STS) of macaque monkeys is thought to be involved in the analysis of incoming perceptual information for face recognition or identification; face neurons in the anterior STS show tuning to facial views and/or gaze direction in the faces of others. Although it is well known that both the anatomical architecture and the connectivity differ between the rostral and caudal regions of the anterior STS, the functional heterogeneity of these regions is not well understood. We recorded the activity of face neurons in the anterior STS of macaque monkeys during the performance of a face identification task, and we compared the characteristics of face neuron responses in the caudal and rostral regions of the anterior STS. In the caudal region, facial views that elicited optimal responses were distributed among all views tested; the majority of face neurons responded symmetrically to right and left views. In contrast, the face neurons in the rostral region responded optimally to a single oblique view; right-left symmetry among the responses of these neurons was less evident. Modulation of the face neuron responses according to gaze direction was more evident in the rostral region. Some of the face neuron responses were specific to a certain combination of a particular facial view and a particular gaze direction, whereas others were associated with the relative spatial relationship between facial view and gaze direction. Taken together, these results indicated the existence of a functional heterogeneity within the anterior STS and suggested a plausible hierarchical organization of facial information processing.

Taking an “intentional stance” on eye-gaze shifts: A functional neuroimaging study of social perception in children

During middle childhood, children develop an increasing understanding of intentions and other social information conveyed through dynamic facial cues such as changes in eye-gaze direction. Recent work in our laboratory has focused on using functional magnetic resonance imaging (fMRI) in adults to map the neural circuitry subserving the visual analysis of others' actions and the intentions underlying these actions. In these studies, the superior temporal sulcus (STS) region has been continually implicated in processing shifts in eye gaze. Further, these studies have indicated that STS activity is modulated by the context within which eye-gaze shifts occur, suggesting that this region is involved in social perception via its role in the analysis of the intentions of observed actions. Still, no studies have investigated the neural circuitry supporting eye-gaze processing in children. We used event-related fMRI to examine brain activity in 7- to 10-year-old healthy children observing an animated virtual actor who shifted her eyes towards either a target object or empty space. Consistent with prior studies in adults, the STS, middle temporal gyrus, and inferior parietal lobule were sensitive to the intentions underlying the stimulus character's eye movements. These findings suggest that the neural circuitry underlying the processing of eye gaze and the detection of intentions conveyed through shifts in eye gaze in children are similar to that found previously in adults. We discuss these findings and potential implications for mapping the neurodevelopment of the social cognition and social perception abnormalities characteristic of autism.

Neural basis of eye gaze processing deficits in autism

Impairments in using eye gaze to establish joint attention and to comprehend the mental states and intentions of other people are striking features of autism. Here, using event-related functional MRI (fMRI), we show that in autism, brain regions involved in gaze processing, including the superior temporal sulcus (STS) region, are not sensitive to intentions conveyed by observed gaze shifts. On congruent trials, subjects watched as a virtual actor looked towards a checkerboard that appeared in her visual field, confirming the subject's expectation regarding what the actor 'ought to do' in this context. On incongruent trials, she looked towards empty space, violating the subject's expectation. Consistent with a prior report from our laboratory that used this task in neurologically normal subjects, 'errors' (incongruent trials) evoked more activity in the STS and other brain regions linked to social cognition, indicating a strong effect of intention in typically developing subjects (n = 9). The same brain regions were activated during observation of gaze shifts in subjects with autism (n = 10), but did not differentiate congruent and incongruent trials, indicating that activity in these regions was not modulated by the context of the perceived gaze shift. These results demonstrate a difference in the response of brain regions underlying eye gaze processing in autism. We conclude that lack of modulation of the STS region by gaze shifts that convey different intentions contributes to the eye gaze processing deficits associated with autism.

Functional Anatomy of Biological Motion Perception in Posterior Temporal Cortex: An fMRI Study of Eye, Mouth and Hand Movements

Passive viewing of biological motion engages extensive regions of the posterior temporal-occipital cortex in humans, particularly within and nearby the superior temporal sulcus (STS). Relatively little is known about the functional specificity of this area. Some recent studies have emphasized the perceived intentionality of the motion as a potential organizing principle, while others have suggested the existence of a somatotopy based upon the limb perceived in motion. Here we conducted an event-related functional magnetic resonance imaging experiment to compare activity elicited by movement of the eyes, mouth or hand. Each motion evoked robust activation in the right posterior temporal-occipital cortex. While there was substantial overlap of the activation maps in this region, the spatial distribution of hemodynamic response amplitudes differentiated the movements. Mouth movements elicited activity along the mid-posterior STS while eye movements elicited activity in more superior and posterior portions of the right posterior STS region. Hand movements activated more inferior and posterior portions of the STS region within the posterior continuing branch of the STS. Hand-evoked activity also extended into the inferior temporal, middle occipital and lingual gyri. This topography may, in part, reflect the role of particular body motions in different functional activities.

Activation in Posterior Superior Temporal Sulcus Parallels Parameter Inducing the Percept of Animacy

An essential, evolutionarily stable feature of brain function is the detection of animate entities, and one of the main cues to identify them is their movement. We developed a model of a simple interaction between two objects, in which an increase of the correlation between their movements varied the amount of interactivity and animacy observers attributed to them. Functional magnetic resonance imaging revealed that activation in the posterior superior temporal sulcus and gyrus (pSTS/pSTG) increased in relation to the degree of correlated motion between the two objects. This activation increase was not different when subjects performed an explicit or implicit task while observing these interacting objects. These data suggest that the pSTS and pSTG play a role in the automatic identification of animate entities, by responding directly to an objective movement characteristic inducing the percept of animacy, such as the amount of interactivity between two moving objects.

Grasping the Intentions of Others: The Perceived Intentionality of an Action Influences Activity in the Superior Temporal Sulcus during Social Perception

An explication of the neural substrates for social perception is an important component in the emerging field of social cognitive neuroscience and is relevant to the field of cognitive neuroscience as a whole. Prior studies from our laboratory have demonstrated that passive viewing of biological motion (Pelphrey, Mitchell, et al., 2003; Puce et al., 1998) activates the posterior superior temporal sulcus (STS ) region. Furthermore, recent evidence has shown that the perceived context of observed gaze shifts (Pelphrey, Singerman, et al., 2003; Pelphrey et al., 2004) modulates STS activity. Here, using event-related functional magnetic resonance imaging at 4 T, we investigated brain activity in response to passive viewing of goal- and nongoal-directed reaching-to-grasp movements. Participants viewed an animated character making reaching-to-grasp movements either toward (correct) or away (incorrect) from a blinking dial. Both conditions evoked significant posterior STS activity that was strongly right lateralized. By examining the time course of the blood oxygenation level-dependent response from areas of activation, we observed a functional dissociation. Incorrect trials evoked significantly greater activity in the STS than did correct trials, while an area posterior and inferior to the STS (likely corresponding to the MT/ V5 complex) responded equally to correct and incorrect movements. Parietal cortical regions, including the superior parietal lobule and the anterior intraparietal sulcus, also responded equally to correct and incorrect movements, but showed evidence for differential responding based on the hand and arm (left or right) of the animated character used to make the reaching-to-grasp movement. The results of this study further suggest that a region of the right posterior STS is involved in analyzing the intentions of other people's actions and that activity in this region is sensitive to the context of observed biological motions.

Neuroanatomical substrates of social cognition dysfunction in autism

In this review article, we summarize recent progress toward understanding the neural structures and circuitry underlying dysfunctional social cognition in autism. We review selected studies from the growing literature that has used the functional neuroimaging techniques of cognitive neuroscience to map out the neuroanatomical substrates of social cognition in autism. We also draw upon functional neuroimaging studies with neurologically normal individuals and individuals with brain lesions to highlight the insights these studies offer that may help elucidate the search for the neural basis of social cognition deficits in autism. We organize this review around key brain structures that have been implicated in the social cognition deficits in autism: (1) the amygdala, (2) the superior temporal sulcus region, and (3) the fusiform gyrus. We review some of what is known about the contribution of each structure to social cognition and then review autism studies that implicate that particular structure. We conclude with a discussion of several potential future directions in the cognitive neuroscience of social deficits in autism.

Is voice processing species-specific in human auditory cortex? An fMRI study

Recent studies suggested a sensitivity of regions of the human superior temporal sulcus (STS) to the sound of the human voice. However, the question of the species specificity of this response is still open. Healthy adult volunteers were scanned in an event-related fMRI design to compare responses in the STS to human and animal vocalizations, as well as to control nonvocal sounds (e.g., musical instruments). Bilateral activation of anterior STS was observed for human vocalizations, when contrasted with both nonvocal sounds and animal vocalizations. Animal vocalizations, compared to nonvocal sounds, elicited a more restricted left STS activation, although this region responded even more strongly to human vocalizations. This study provides the first evidence suggesting a species specificity in STS responses to vocalizations in humans.

Source analysis of the N170 to faces and objects.

To clarify the neural sources for the face-sensitive N170, ERPs were recorded in 16 subjects viewing upright and inverted faces, and compared to seven object categories. Source analyses were performed for each category and each subject at the latency of the N170. Larger source intensities were found in the posterior superior temporal sulcus region (STS) for faces compared to objects. STS intensities were highly correlated to the N170 amplitude over both hemispheres only for faces. The results suggest that one of the major sources of the N170 is the STS region and that the larger N170 amplitude to inverted faces is due to increased activation of that source for inverted faces rather than a recruitment of additional areas.