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The ability to extract the direction of the other's gaze allows us to shift our attention to an object of interest to the other and to establish joint attention. By mapping one's own intentions on the object of joint attention, humans develop a Theory of (the other's) Mind (TOM), a functional sequence possibly disrupted in autism. Gaze following of both humans and old world monkeys is orchestrated by very similar cortical architectures, strongly suggesting homology. Also new world monkeys, a primate suborder that split from the old world monkey line about 35 million years ago, have complex social structures and one member of this group, the common marmosets (Callithrix jacchus) are known to follow human head-gaze. However, the question is if they use gaze following to establish joint attention with conspecifics. Here we show that this is indeed the case. In a free choice task, head-restrained marmosets prefer objects gazed at by a conspecific and, moreover, they exhibit considerably shorter choice reaction times for the same objects. These findings support the assumption of an evolutionarily old domain specific faculty shared within the primate order and they underline the potential value of marmosets in studies of normal and disturbed joint attention.

Humans follow another person's eye gaze to objects of interest to the other, thereby establishing joint attention, a first step toward developing a theory of the other's mind. Previous functional MRI studies agree that a "gaze-following patch" (GFP) of cortex close to the posterior superior temporal sulcus (STS) is specifically implicated in eye gaze-following. The location of the GFP is in the vicinity of the posterior members of the core face-processing system that consists of distinct patches in ventral visual cortex, the STS, and frontal cortex, also involved in processing information on the eyes. To test whether the GFP might correspond to one of the posterior face patches, we compared the pattern of blood oxygenation level-dependent (BOLD) imaging contrasts reflecting the passive vision of static faces with the one evoked by shifts of attention guided by the eye gaze of others. The viewing of static faces revealed the face patch system. On the other hand, eye gaze-following activated a cortical patch (the GFP) with its activation maximum separated by more than 24 mm in the right and 19 mm in the left hemisphere from the nearest face patch, the STS face area (FA). This segregation supports a distinct function of the GFP, different from the elementary processing of facial information., Competing Interests: Authors report no conflict of interest.

Human eye-gaze is a powerful stimulus, drawing the observer's attention to places and objects of interest to someone else ('eye-gaze following'). The largely homogeneous eyes of monkeys, compromising the assessment of eye-gaze by conspecifics from larger distances, explain the absence of comparable eye-gaze following in these animals. Yet, monkeys are able to use peer head orientation to shift attention ('head-gaze following'). How similar are monkeys' head-gaze and human eye-gaze following? To address this question, we trained rhesus monkeys to make saccades to targets, either identified by the head-gaze of demonstrator monkeys or, alternatively, identified by learned associations between the demonstrators' facial identities and the targets (gaze versus identity following). In a variant of this task that occurred at random, the instruction to follow head-gaze or identity was replaced in the course of a trial by the new rule to detect a change of luminance of one of the saccade targets. Although this change-of-rule rendered the demonstrator portraits irrelevant, they nevertheless influenced performance, reflecting a precise redistribution of spatial attention. The specific features depended on whether the initial rule was head-gaze or identity following: head-gaze caused an insuppressible shift of attention to the target gazed at by the demonstrator, whereas identity matching prompted much later shifts of attention, however, only if the initial rule had been identity following. Furthermore, shifts of attention prompted by head-gaze were spatially precise. Automaticity and swiftness, spatial precision and limited executive control characterizing monkeys' head-gaze following are key features of human eye-gaze following. This similarity supports the notion that both may rely on the same conserved neural circuitry., (© 2015 The Author(s).)

Despite the ecological importance of gaze following, little is known about the underlying neuronal processes, which allow us to extract gaze direction from the geometric features of the eye and head of a conspecific. In order to understand the neuronal mechanisms underlying this ability, a careful description of the capacity and the limitations of gaze following at the behavioral level is needed. Previous studies of gaze following, which relied on naturalistic settings have the disadvantage of allowing only very limited control of potentially relevant visual features guiding gaze following, such as the contrast of iris and sclera, the shape of the eyelids and--in the case of photographs--they lack depth. Hence, in order to get full control of potentially relevant features we decided to study gaze following of human observers guided by the gaze of a human avatar seen stereoscopically. To this end we established a stereoscopic 3D virtual reality setup, in which we tested human subjects' abilities to detect at which target a human avatar was looking at. Following the gaze of the avatar showed all the features of the gaze following of a natural person, namely a substantial degree of precision associated with a consistent pattern of systematic deviations from the target. Poor stereo vision affected performance surprisingly little (only in certain experimental conditions). Only gaze following guided by targets at larger downward eccentricities exhibited a differential effect of the presence or absence of accompanying movements of the avatar's eyelids and eyebrows., (Copyright © 2015 Elsevier Ltd. All rights reserved.)

Distinguishing a target from distractors during visual search is crucial for goal-directed behaviour. The more distractors that are presented with the target, the larger is the subject's error rate. This observation defines the set-size effect in visual search. Neurons in areas related to attention and eye movements, like the lateral intraparietal area (LIP) and frontal eye field (FEF), diminish their firing rates when the number of distractors increases, in line with the behavioural set-size effect. Furthermore, human imaging studies that have tried to delineate cortical areas modulating their blood oxygenation level-dependent (BOLD) response with set size have yielded contradictory results. In order to test whether BOLD imaging of the rhesus monkey cortex yields results consistent with the electrophysiological findings and, moreover, to clarify if additional other cortical regions beyond the two hitherto implicated are involved in this process, we studied monkeys while performing a covert visual search task. When varying the number of distractors in the search task, we observed a monotonic increase in error rates when search time was kept constant as was expected if monkeys resorted to a serial search strategy. Visual search consistently evoked robust BOLD activity in the monkey FEF and a region in the intraparietal sulcus in its lateral and middle part, probably involving area LIP. Whereas the BOLD response in the FEF did not depend on set size, the LIP signal increased in parallel with set size. These results demonstrate the virtue of BOLD imaging in monkeys when trying to delineate cortical areas underlying a cognitive process like visual search. However, they also demonstrate the caution needed when inferring neural activity from BOLD activity., (© 2013 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.)

Visual scenes explored covertly are initially represented in a retinal frame of reference (FOR). On the other hand, 'later' stages of the cortical network allocating spatial attention most probably use non-retinal or non-eye-centred representations as they may ease the integration of different sensory modalities for the formation of supramodal representations of space. We tested if the cortical areas involved in shifting covert attention are based on eye-centred or non-eye-centred coding by using functional magnetic resonance imaging. Subjects were scanned while detecting a target item (a regularly oriented 'L') amidst a set of distractors (rotated 'L's). The array was centred either 5° right or left of the fixation point, independent of eye-gaze orientation, the latter varied in three steps: straight relative to the head, 10° left or 10° right. A quantitative comparison of the blood-oxygen-level-dependent (BOLD) responses for the three eye-gaze orientations revealed stronger BOLD responses in the right intraparietal sulcus (IPS) and the right frontal eye field (FEF) for search in the contralateral (i.e. left) eye-centred space, independent of whether the array was located in the right or left head-centred hemispace. The left IPS showed the reverse pattern, i.e. an activation by search in the right eye-centred hemispace. In other words, the IPS and the right FEF, members of the cortical network underlying covert search, operate in an eye-centred FOR., (© 2013 Federation of European Neuroscience Societies and Blackwell Publishing Ltd.)

Previous fMRI experiments showed an involvement of the STS in the processing of eye-gaze direction in joint attention. Since head-gaze direction can also be used for the assessment of another person's attentional focus, we compared the mechanisms underlying the processing of head- and eye-gaze direction using a combined psychophysical and fMRI approach. Subjects actively followed the head- or eye-gaze direction of a person in a photograph towards one of seven possible targets by moving their eyes. We showed that the right posterior superior temporal sulcus (STS) as well as the right fusiform gyrus (FSG) were involved in both processing of head- as well as eye-gaze direction. Another finding was a bilateral deactivation of a distinct area in the middle STS (mSTS) as well as the left anterior STS (aSTS), that was stronger when subjects followed eye-gaze direction than when they followed head-gaze direction. We assume that this deactivation is based on an active suppression of information arising from the distracting other directional cue, i.e. head-gaze direction in the eye-gaze direction task and eye-gaze direction in the head-gaze direction task. These results further support the hypothesis that the human equivalent of the gaze sensitive area in monkeys lies in more anterior parts of the STS than previously thought., (Copyright © 2010 Elsevier Inc. All rights reserved.)

Lesions of the cerebellum produce deficits in movement and motor learning. Saccadic dysmetria, for example, is caused by lesions of the posterior cerebellar vermis. Monkeys and patients with such lesions are unable to modify the amplitude of saccades. Some have suggested that the effects on eye movements might reflect a more global cognitive deficit caused by the cerebellar lesion. We tested that idea by studying the effects of vermis lesions on attention as well as saccadic eye movements, visual motion perception, and luminance change detection. Lesions in posterior vermis of four monkeys caused the known deficits in saccadic control. Attention tested by examination of acuity threshold changes induced by prior cueing of the location of the targets remained normal after vermis lesions. Luminance change detection was also unaffected by the lesions. In one case, after a lesion restricted to lobulus VIII, the animal had impaired visual motion perception.

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.

The analysis of a peripheral visual location can be improved in two ways: either by orienting one's gaze (usually by making a foveating saccade) or by 'covertly' shifting one's attention to the peripheral location without making an eye movement. The premotor theory of attention holds that saccades and spatial shifts of attention share a common functional module with a distinct neuronal basis. Using single-unit recording from the brains of trained rhesus monkeys, we investigated whether the superior colliculus, the major subcortical center for the control of saccades, is part of this shared network for attention and saccades. Here we show that a distinct type of neuron in the intermediate layer of the superior colliculus, the visuomotor neuron, which is known to be centrally involved in the preparation of saccades, is also active during covert shifts of attention.