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.

Visual attention and action: How cueing, direct mapping, and social interactions drive orienting

“…Although the IPS has generally been shown to undergo greater activation following averted rather than direct gaze (i.e., when gaze is directed at the observer; Hoffman & Haxby, 2000), unlike the STS it is not thought to be sensitive to biological cues. Both socially relevant and nonsocially relevant directional judgments have been found to elicit activation in this area (Materna et al, 2008).…”

“…M. Tipper, Handy, Giesbrecht, & Kingstone, 2008). The STS has dense connections to the intraparietal sulcus (IPS), which is important in covert attention shifts and spatial processing (Corbetta et al, 1998;Harries & Perrett, 1991;Materna, Dicke, & Thier, 2008;Rafal, 1996). The role of these connections has found support in studies that have correlated STS activation with activity in IPS under conditions where averted gaze (i.e., where gaze is directed away from the observer) is viewed (George, Driver, & Dolan, 2001;Pelphrey, Singerman, Allison, & McCarthy, 2003;Wicker, Michel, Henaff, & Decety, 1998).…”

Mirroring of attention by neurons in macaque parietal cortex

“…Thus, although neuroimaging techniques can identify cortical areas sensitive to the direction of observed gaze, their temporal resolution is too coarse to determine whether these areas are capable of mediating fast gaze-following behavior. To date, the neural correlates of social gaze-evoked attention have only been explored by using brain imaging or neuropsychological techniques in humans (35)(36)(37).…”

Optical imaging of the prefrontal activity in joint attention experience

“…Meanwhile, the social relatedness and relationships of adolescents and even adults would be impaired if they lack of the ability to share attention in social interactions. In addition to behavioral observation, neuroimaging methods were used to reveal brain substrate underlying joint attention process [8][9][10][11][12]. The physiological information obtained from imaging techniques, together with behavioral observation, would help psychologists or neuroscientists achieve a more comprehensive understanding on joint attention.…”

“…The physiological information obtained from imaging techniques, together with behavioral observation, would help psychologists or neuroscientists achieve a more comprehensive understanding on joint attention. The mostly used neuroimaging techniques in joint attention study are electroencephalography (EEG) and functional magnetic resonance imaging (fMRI), the former technique was used for infants [8,9], while the later for adults [10][11][12]. The convergent evidence from joint attention studies on subjects at different developmental stage (infancy, adulthood) with different imaging modalities (EEG, fMRI) show that joint attention process is associated with the anterior and posterior attention system [10,13,14], the former system includes the frontal eye fields, anterior cingulate and orbital prefrontal cortex, while the later includes the superior parietal lobule, inferior parietal lobule, middle temporal gyrus, and superior temporal gyrus.…”