For humans, being looked at directly can boost our readiness to follow another’s gaze, but can monkeys invite an observer to engage with them in the same way? We trained three rhesus macaques on a head gaze-following task in which the portrait of a demonstrator monkey would face the viewer before turning to look at a distinct spatial target. The demonstrator could face the viewer with their eyes opened or closed and display different facial expressions. Unlike in humans, we found that direct gaze alone, devoid of an accompanying specific expression failed to influence the latency of the subsequent gaze-following response. However, when combined with threat, direct gaze significantly accelerated gaze-following. In a second experiment, we show that once turned away the expression associated with prior direct gaze no longer mattered; instead a submissive facial expression accompanying the gaze shift delayed gaze-following. Direct comparison of both experiments reveals that expressions accompanying direct gaze trigger earlier gaze-following responses than the same expressions joining gaze aversion. These results document the behavioral relevance of threat-related facial expressions for gaze-following in rhesus macaques, with expressions that signal conflict selectively expediting orienting responses.

Abstract Previous research suggests that humans are extremely sensitive to object-directed eye gaze, which effectively guides their attention toward objects of shared interest. This contrasts with non-human primates, who typically require much more salient eye-gaze cues to achieve comparable attentional orienting. However, it remains unclear whether cross-species differences in ocular morphology account for this performance gap. To address this question, we examined humans’ covert shifts of spatial attention in response to eye-gaze cues provided by either realistic human or rhesus monkey head avatars. Target detection was reliably enhanced on gaze-congruent compared to gaze-incongruent trials, with comparable gaze-cueing effects for both avatar types, despite the fact that monkey eyes lack many of the conspicuous features characteristic of human eyes. Hence, eye morphology alone does not substantially modulate gaze-driven attentional orienting in humans, whereas humans’ reliable use of monkey eye-gaze cues highlights a clear species difference in perceptual sensitivity to eye gaze signals. Significance Statement Eye-gaze–mediated attentional orienting is a conserved ability across primates, yet sensitivity to subtle eye-gaze cues may differ between species. Here, we provide empirical evidence that humans exhibit a quantitatively greater capacity than non-human primates to follow subtle eye-gaze cues. Importantly, we showed that this difference cannot be attributed to species-specific ocular morphology as human participants showed robust and comparable reflexive attentional orienting to both human and rhesus monkey eye-gaze cues. This is striking given the pronounced differences in ocular morphology and coloration/contrast between the two species. These findings suggest that cross-species diversity in extracting spatial information from eye-gaze cues likely reflects differences in perceptual sensitivity rather than bottom-up constraints imposed by species-specific ocular morphology.

Nonverbal cues, particularly eye-gaze, significantly shape human social interactions. Although nonhuman primates reliably follow head gaze, their capacity to use eye-gaze alone for inferring the other’s focus of attention remains debated. We investigated this question using a realistic rhesus monkey head avatar that directed its gaze toward one of two LEDs (left or right), employing either eye movements alone or combined eye and head movements. After a randomly chosen interval (range: 50–400 ms) from gaze presentation, one LED transiently increased its luminance to near-threshold levels. Rhesus monkeys were trained to detect and report this luminance change via a saccade to the corresponding LED, independent of the avatar’s gaze direction, to receive rewards. Our results showed that head-gaze cues robustly directed covert attention toward gaze-congruent targets with short delays, indicative of reflex-like, stimulus-driven orienting. In contrast, eye-gaze alone, at comparable amplitudes, did not affect attentional shifts. However, increasing the avatar’s size and eye-gaze amplitude, simulating a close-range interaction, made eye-gaze cues effective in guiding attention. These findings demonstrate that rhesus monkeys possess the capacity to use eye-gaze cues to determine conspecifics’ attentional targets, and validate and underscore the utility of 3D animal models as powerful tools for generating realistic yet precisely controlled stimuli. Our study supports the idea that eye-gaze following is not uniquely human but is an evolutionarily ancient ability, likely shared across Old World monkeys and apes that diverged more than 30 million years ago.

Abstract The ventral premotor cortex (PMv) has been implicated in both action selection and the perception of observed actions, but it remains unclear whether PMv activity during action observation reflects the observed action itself, or variables related to the observer’s own action when the observed action becomes behaviourally relevant. Here, we recorded neural activity in macaque PMv during a task that dissociated observed action, rule context, and the subsequently selected self-action. Population activity during observation was already biased toward the upcoming self-action and became increasingly aligned with it. At the level of single neurons, subsets showed modulation by rule and required self-action beyond the observed action. Task-related variables coexisted during observation, rather than being organized into distinct sequential stages. These findings indicate that PMv activity during action observation is not solely determined by the observed action, but instead reflects variables related to the selection of the agent’s own action, consistent with a transformation from observed action to self-action.

Short-term motor adaptation is a form of motor learning that optimizes how sensory information about a target's location is translated into a target-directed movement, using sensory feedback on performance errors. When actual and predicted sensory feedback differ, sensory prediction errors (SPEs) are generated, enabling the cerebellum to adjust this mapping. In contrast, reinforcement learning uses reward prediction error (RPEs) based on fulfilled or unfulfilled reward expectations to shape future actions. As RPE-related information also reaches the cerebellum, we wondered whether it interacts with SPEs to shape short-term motor adaptation. We addressed this in monkeys by inducing visual errors via inward and outward intra-saccadic target steps, generating corresponding SPEs and quantifying adaptation as changes in saccade amplitude across same-direction trials before and after SPEs. In two separate studies, we manipulated information about trial outcomes (reward versus no reward) to examine its interaction with SPEs in saccadic adaptation. In both, we found that RPEs modulate single-trial saccadic adaptation. Sensory errors determined the direction of adaptation, whereas reward-related signals scaled its magnitude, revealing an interaction between SPEs and RPEs in trial-by-trial motor learning and underscoring the behavioural relevance of their co-representation in shared cerebellar afferents.

BACKGROUND:Electrocorticography (ECoG) provides a valuable compromise between spatial and temporal resolution for recording brain activity with excellent signal quality, crucial for presurgical epilepsy mapping and advancing neuroscience, including brain-machine interface development. ECoG is particularly effective in the common marmoset (Callithrix jacchus), whose lissencephalic (unfolded) brain surface provides broad cortical access. One of the key advantages of ECoG recordings is the ability to study interactions between distant brain regions. Traditional methods rely on large electrode arrays, necessitating extensive trepanations and a trade-off between size and electrode spacing. NEW METHOD:This study introduces a refined ECoG technique for examining interactions among multiple cortical areas in marmosets, combining circumscribed trepanations with high-density electrode arrays at specific sites of interest. COMPARISON WITH EXISTING METHODS:Standard ECoG techniques typically require large electrode arrays and extensive trepanation, which heighten surgical risks and the likelihood of infection, while potentially compromising spatial resolution. In contrast, our method facilitates detailed and stable recordings across multiple cortical areas with minimized invasiveness and reduced complication risks, all while preserving high spatial resolution. RESULTS:Two adult marmosets underwent ECoG implantation in frontal, temporal, and parietal regions. Postoperative monitoring confirmed rapid recovery, long-term health, and stable, high-quality neural recordings during various behavioral tasks. CONCLUSIONS:This refined ECoG method enhances the study of cortical interactions in marmosets while minimizing surgical invasiveness and complication risks. It offers potential for broader application in other species and opens new avenues for long-term data collection, ultimately advancing both neuroscience and brain-machine interface research.

Apart from language, our gaze is arguably the most important means of communication. Where we look lets others know what we are interested in and allows them to join our focus of attention. In several studies our group investigated the neuronal basis of gaze following behavior in humans and macaques and described a gaze following patch (GFP) in the posterior temporal cortex as being of central importance for this function. To our knowledge, this makes the GFP the most promising neurobiological correlate of Simon Baron-Cohen’s eye direction detector (EDD), an integral part of his influential mindreading system. With the latter, Baron-Cohen proposed a set of domain-specific neurocognitive modules implementing a functional framework he suggested to be necessary to establish a Theory of Mind - the attribution of mental states to others. The tenet of domain-specificity requires that the EDD processes only and exclusively eye-like stimuli with their typical contrast and movement properties. In this preregistered fMRI study, we aimed to critically test if the GFP fulfills this criterion. Specifically, we tested if it is equivalent to or different from the visual motion processing areas located in the same part of the brain. Contrary to previous studies, the present results clearly demonstrate that GFP activity is not exclusively correlated with the perception of other people’s gaze direction and thus does not fulfill the criterion of domain-specificity. Furthermore, we show that it cannot be functionally dissociated from the MT+ complex, with which it overlaps anatomically. Given that our experiments captured the full extent of gaze-following behavior and were specifically designed to reveal an EED, our results provide evidence against its existence, and therefore against Baron-Cohen's mindreading model as a set of domain-specific modules.

The gaze beam hypothesis ( GBH ) of gaze following posits that the other's eyes emit imaginary beams of moving energy travelling to the other's object of attention, drawing the observer's attention to the same object. This idea was initially supported by behavioral experiments showing a motion aftereffect ( MAE ), indicated by longer reaction times in detecting motion direction after viewing a cartoon face looking at an object in the same direction. However, this effect could also be expected if the observer used gaze direction to assume an intentional link between the looker and the object, envisioning directed actions toward the latter. To critically compare the two hypotheses, we tested whether an MAE could be induced by having human subjects detect motion direction after viewing various cue images, designed to differentiate the explanatory power of the two. Cues either suggested a connection between an agent and an object through the agent's gaze or an object-oriented intention by the presence of equipment in the agent's hand, without the agent directly looking at the object. Using Bayesian statistics, our findings provided strong evidence against both hypotheses at the population level, as reaction time modulations did not align with the MAE , leading us to reject motion adaptation as the underlying mechanism for gaze following but also intention attribution. As on an individual level we observed highly diverse effects, with some compatible with one or the other hypothesis, we assume that individual subjects may resort to different perceptual strategies based on different scene interpretations. ### Competing Interest Statement The authors have declared no competing interest.

The gaze-following patch (GFP) is located in the posterior temporal cortex and has been described as a cortical module dedicated to processing other people's gaze-direction in a domain-specific manner. Thus, it appears to be the neural correlate of Baron-Cohen's eye direction detector (EDD) which is one of the core modules in his mindreading system-a neurocognitive model for the theory of mind concept. Inspired by Jerry Fodor's ideas on the modularity of the mind, Baron-Cohen proposed that, among other things, the individual modules are domain specific. In the case of the EDD, this means that it exclusively processes eye-like stimuli to extract gaze-direction and that other stimuli, which may carry directional information as well, are processed elsewhere. If the GFP is indeed EDD's neural correlate, it must meet this expectation. To test this, we compared the GFP's BOLD activity during gaze-direction following with the activity during arrow-direction following in the present human fMRI study. Contrary to the expectation based on the assumption of domain specificity, we did not find a differentiation between gaze- and arrow-direction following. In fact, we were not able to reproduce the GFP as presented in the previous studies. A possible explanation is that in the present study-unlike the previous work-the gaze stimuli did not contain an obvious change of direction that represented a visual motion. Hence, the critical stimulus component responsible for the identification of the GFP in the previous experiments might have been visual motion.

Both the environment and our body keep changing dynamically. Hence, ensuring movement precision requires adaptation to multiple demands occurring simultaneously. Here we show that the cerebellum performs the necessary multi-dimensional computations for the flexible control of different movement parameters depending on the prevailing context. This conclusion is based on the identification of a manifold-like activity in both mossy fibers (MFs, network input) and Purkinje cells (PCs, output), recorded from monkeys performing a saccade task. Unlike MFs, the PC manifolds developed selective representations of individual movement parameters. Error feedback-driven climbing fiber input modulated the PC manifolds to predict specific, error type-dependent changes in subsequent actions. Furthermore, a feed-forward network model that simulated MF-to-PC transformations revealed that amplification and restructuring of the lesser variability in the MF activity is a pivotal circuit mechanism. Therefore, the flexible control of movements by the cerebellum crucially depends on its capacity for multi-dimensional computations.

Gaze-following, the ability to shift one’s own attention to places or objects others are looking at, is essential for social interactions. Single unit recordings from the monkey cortex and neuroimaging work on the human and monkey brain suggest that a distinct region in the temporal cortex, the gaze-following patch (GFP), underpins this ability. Since previous studies of the GFP have relied on correlational techniques, it remains unclear whether gaze-following related activity in the GFP indicates a causal role rather than being just a reverberation of behaviorally relevant information produced elsewhere. To answer this question, we applied focal electrical and pharmacological perturbation to the GFP. Both approaches, when applied to the GFP, disrupted gaze-following if the monkeys had been instructed to follow gaze, along with the ability to suppress it if vetoed by the context. Hence the GFP is necessary for gaze-following as well as its cognitive control.

According to the mirror mechanism the discharge of F5 mirror neurons of a monkey observing another individual performing an action is a motor representation of the observed action that may serve to understand or learn from the action. This hypothesis, if strictly interpreted, requires mirror neurons to exhibit an action tuning that is shared between action observation and execution. Due to insufficient data it remains contentious if this requirement is met. To fill in the gaps, we conducted an experiment in which identical objects had to be manipulated in three different ways in order to serve distinct action goals. Using three methods, including cross-task classification, we found that at most time points F5 mirror neurons did not encode observed actions with the same code underlying action execution. However, in about 20% of neurons there were time periods with a shared code. These time periods formed a distinct cluster and cannot be considered a product of chance. Population classification yielded non-shared coding for observed actions in the whole population, which was at times optimal and consistently better than shared coding in differentially selected subpopulations. These results support the hypothesis of a representation of observed actions based on a strictly defined mirror mechanism only for small subsets of neurons and only under the assumption of time-resolved readout. Considering alternative concepts and recent findings, we propose that during observation mirror neurons represent the process of a goal pursuit from the observer's viewpoint. Whether the observer's goal pursuit, in which the other's action goal becomes the observer's action goal, or the other's goal pursuit is represented remains to be clarified. In any case, it may allow the observer to use expectations associated with a goal pursuit to directly intervene in or learn from another's action.

When human subjects tilt their heads in dark surroundings, the noisiness of vestibular information impedes precise reports on objects’ orientation with respect to earth’s vertical axis. This difficulty is mitigated if a vertical visual background is available. Tilted visual backgrounds induce feelings of head tilt in subjects who are in fact upright. This is often explained as a result of the brain resorting to the prior assumption that natural visual backgrounds are vertical. Here, we tested whether monkeys show comparable perceptual mechanisms. To this end we trained two monkeys to align a visual arrow to a vertical reference line that had variable luminance across trials, while including a large, clearly visible background square whose orientation changed from trial to trial. On around 20% of all trials, the vertical reference line was left out to measure the subjective visual vertical ( SVV ). When the frame was upright, the monkeys’ SVV was aligned with the gravitational vertical. In accordance with the perceptual reports of humans, however, when the frame was tilted, it induced an illusion of head tilt as indicated by a bias in SVV towards the frame orientation. Thus all primates exploit the prior assumption that the visual world is vertical.

We studied neurons in the brain’s frontal eye field (FEF) to understand how these neurons predict swift eye shifts called saccades. We found that neurons with more movement-related activity were better at predicting saccades than those with sensory-related activity. Interestingly, electrical disruptions of this region strongly impacted saccade onset times but did not affect the individual neuron’s saccade predictability, consistent with models suggesting that a specific threshold in neural activity triggers the saccade.

Gaze following is a major element of non-verbal communication and important for successful social interactions. Human gaze following is a fast and almost reflex-like behaviour, yet it can be volitionally controlled and suppressed to some extent if inappropriate or unnecessary, given the social context. In order to identify the neural basis of the cognitive control of gaze following, we carried out an event-related fMRI experiment, in which human subjects' eye movements were tracked while they were exposed to gaze cues in two distinct contexts: A baseline gaze following condition in which subjects were instructed to use gaze cues to shift their attention to a gazed-at spatial target and a control condition in which the subjects were required to ignore the gaze cue and instead to shift their attention to a distinct spatial target to be selected based on a colour mapping rule, requiring the suppression of gaze following. We could identify a suppression-related blood-oxygen-level-dependent (BOLD) response in a frontoparietal network comprising dorsolateral prefrontal cortex (dlPFC), orbitofrontal cortex (OFC), the anterior insula, precuneus, and posterior parietal cortex (PPC). These findings suggest that overexcitation of frontoparietal circuits in turn suppressing the gaze following patch might be a potential cause of gaze following deficits in clinical populations.

Apart from language, our gaze is arguably the most important means of communication. Where we look lets others know what we are interested in and allows them to join our focus of attention. In several studies our group investigated the neuronal basis of gaze following behavior in humans and macaques and described the Gaze following patch in the posterior temporal cortex as being of central importance for this function. To our knowledge, this makes it the most promising candidate for Simon Baron-Cohen’s Eye-Direction-Detector , an integral part of his influential Mindreading System. With the latter, Baron-Cohen proposed a network of domain-specific neurocognitive modules that are necessary to establish a Theory of Mind - the attribution of mental states to others. The tenet of domain-specificity requires that the EDD processes only and exclusively eye-like stimuli with their typical contrast and movement properties. In the present fMRI study, we aim to critically test if the GFP fulfills this criterion. Specifically, we will test if it is equivalent to or different from the visual motion processing areas located in the same part of the brain. Since our experiments capture the full-behavioral relevance of gaze-following behavior and are specifically designed to reveal an EED our results will provide strong support or rejection of a central property Baron-Cohen’s Mindreading-System – domain specificity .