The role of the amygdala in face perception and evaluation

Faces are one of the most significant social stimuli and the processes underlying face perception are at the intersection of cognition, affect, and motivation. Vision scientists have had a tremendous success of mapping the regions for perceptual analysis of faces in posterior cortex. Based on evidence from (a) single unit recording studies in monkeys and humans; (b) human functional localizer studies; and (c) meta-analyses of neuroimaging studies, I argue that faces automatically evoke responses not only in these regions but also in the amygdala. I also argue that (a) a key property of faces represented in the amygdala is their typicality; and (b) one of the functions of the amygdala is to bias attention to atypical faces, which are associated with higher uncertainty. This framework is consistent with a number of other amygdala findings not involving faces, suggesting a general account for the role of the amygdala in perception.     

Brain activity for visual judgment of lifted weight

It is well established that humans can recognize high-level aspects from point-light biological motion, such as gender and mood. If the task is to judge the manipulated weight we expected that sensorimotor regions should be recruited in the brain. Moreover, we have recently shown that chronic pain in a limb that is involved in the presented movement disturbs the weight judgment. We therefore hypothesized that some cortical regions usually activated during the processing of pain will also be activated while viewing point-light biological motion with the instruction to judge the manipulated weights. We investigated point-light biological motion of two types of movements performed with different weights in a blocked fMRI experiment in healthy subjects. In line with our a priori hypothesis, we found strong activity in the regions known as the neuromatrix of pain, such as the anterior cingulate (ACC), insula, as well as primary and secondary somatosensory regions. We also found activation in the occipital and temporal regions that are typical for biological motion, as well as regions in the cerebellum and prefrontal cortex. The activation of the somatosensory regions probably serves the judgment of the biological motion stimuli. Activation of the anterior cingulate and the insula might be explained by their role in the integration of behaviorally relevant information. Alternatively, these structures are known to be involved in the processing of nociceptive information and pain. So it seems possible that the interference between judgment of weights and perception of pain in chronic pain patients occurs in the somatosensory areas, anterior cingulate and/or insula. This finding provides important information as to the underlying mechanisms used for the weight judgment task, but also why chronic pain interferes with this task.     

Processing the facial image: a brief history

The study of the neural basis of face perception is a major research interest today. This review traces its roots in monkey neuropsychology and neurophysiology beginning with the Klüver-Bucy syndrome and its fractionation and then continuing with lesion and single neuron recording studies of inferior temporal cortex. The context and consequence of the discovery of inferior temporal neurons selective for faces is described and current lines of research on inferior temporal cortex and face processing in both monkeys and humans are outlined.     

Visual motion integration for perception and pursuit

To examine the relationship between visual motion processing for perception and pursuit, we measured the pursuit eye-movement and perceptual responses to the same complex-motion stimuli. We show that humans can both perceive and pursue the motion of line-figure objects, even when partial occlusion makes the resulting image motion vastly different from the underlying object motion. Our results show that both perception and pursuit can perform largely accurate motion integration, i.e. the selective combination of local motion signals across the visual field to derive global object motion. Furthermore, because we manipulated perceived motion while keeping image motion identical, the observed parallel changes in perception and pursuit show that the motion signals driving steady-state pursuit and perception are linked. These findings disprove current pursuit models whose control strategy is to minimize retinal image motion, and suggest a new framework for the interplay between visual cortex and cerebellum in visuomotor control.     

Conserved evolutionary history for quick detection of threatening faces

Humans quickly recognize threats such as snakes and threatening faces, suggesting that human ancestors evolved specialized visual systems to detect biologically relevant threat stimuli. Although non-human primates also detect snakes quickly, it is unclear whether primates share the efficient visual systems to process the threatening faces of their conspecifics. Primates may not necessarily process conspecific threats by facial expressions, because threats from conspecifics in natural situations are often accompanied by other cues such as threatening actions (or attacks) and vocal calls. Here, we show a similar threat superiority effect in both humans and macaque Japanese monkeys. In visual search tasks, monkeys and humans both responded to pictures of a threatening face of an unfamiliar adult male monkey among neutral faces faster than to pictures of a neutral face among threatening faces. However, the monkeys’ response times to detect deviant pictures of a non-face stimulus were not slower when it was shown among threat faces than when it was shown among neutral faces. These results provide the first evidence that monkeys have an attentional bias toward the threatening faces of conspecifics and suggest that threatening faces are evolutionarily relevant fear stimuli. The subcortical visual systems in primates likely process not only snakes, but also more general biological threat-relevant stimuli, including threatening conspecific faces.     

Eye movements of monkey observers viewing vocalizing conspecifics

Primates, including humans, communicate using facial expressions, vocalizations and often a combination of the two modalities. For humans, such bimodal integration is best exemplified by speech-reading - humans readily use facial cues to enhance speech comprehension, particularly in noisy environments. Studies of the eye movement patterns of human speech-readers have revealed, unexpectedly, that they predominantly fixate on the eye region of the face as opposed to the mouth. Here, we tested the evolutionary basis for such a behavioral strategy by examining the eye movements of rhesus monkeys observers as they viewed vocalizing conspecifics. Under a variety of listening conditions, we found that rhesus monkeys predominantly focused on the eye region versus the mouth and that fixations on the mouth were tightly correlated with the onset of mouth movements. These eye movement patterns of rhesus monkeys are strikingly similar to those reported for humans observing the visual components of speech. The data therefore suggest that the sensorimotor strategies underlying bimodal speech perception may have a homologous counterpart in a closely related primate ancestor.     

Intact visual perceptual discrimination in humans in the absence of perirhinal cortex

While the role of the perirhinal cortex in declarative memory has been well established, it has been unclear whether the perirhinal cortex might serve an additional nonmnemonic role in visual perception. Evidence that the perirhinal cortex might be important for visual perception comes from a recent report that monkeys with perirhinal cortical lesions are impaired on difficult (but not on simple) visual discrimination tasks. We administered these same tasks to nine amnesic patients, including three severely impaired patients with complete damage to perirhinal cortex bilaterally (E.P., G.P., and G.T.). The patients performed all tasks as well as controls. We suggest that the function of perirhinal cortex as well as antero-lateral temporal cortex may differ between humans and monkeys.     

Demystifying social cognition: a Hebbian perspective

For humans and monkeys, understanding the actions of others is central to survival. Here we review the physiological properties of three cortical areas involved in this capacity: the STS, PF and F5. Based on the anatomical connections of these areas, and the Hebbian learning rule, we propose a simple but powerful account of how the monkey brain can learn to understand the actions of others by associating them with self-produced actions, at the same time discriminating its own actions from those of others. As this system appears also to exist in man, this network model can provide a framework for understanding human social perception.     

Discrimination of faces and houses by rhesus monkeys: the role of stimulus expertise and rotation angle

The face inversion effect, or impaired recognition of upside down compared to upright faces, is used as a marker for the configural processing of faces in primates. The inversion effect in humans and chimpanzees is strongest for categories of stimuli for which subjects have considerable expertise, primarily conspecifics’ faces. Moreover, discrimination performance decreases linearly as faces are incrementally rotated from upright to inverted. This suggests that rotated faces must be transformed, or normalized back into their most typical viewpoint before configural processing can ensue, and the greater the required normalization, the greater the likelihood of errors resulting. Previous studies in our lab have demonstrated a general face inversion effect in rhesus monkeys that was not influenced by expertise. Therefore, the present study examined the influence of rotation angle on the visual perception of face and nonface stimuli that varied in their level of expertise to further delineate the processes underlying the inversion effect in rhesus monkeys. Five subjects discriminated images in five orientation angles. Results showed significant linear impairments for all stimulus categories, including houses. However, compared to the upright images, only rhesus faces resulted in worse performance at rotation angles greater than 45°, suggesting stronger configural processing for stimuli for which subjects had the greatest expertise.     

从面孔模块到马赛克──视觉特异性加工的脑机制

“脑功能的模块性”是视觉乃至整个认知神经科学的研究热点。特异性的面孔加工模块被当作是认知模块假说的最好证据。但综述跨学科的正反两方面实验证据表明,视觉加工存在特异性,并没有普遍的模块式的亚单元,而是“马赛克”镶嵌式的组构。     

具身认知视角下语义理解中的身体角色:以研究方法为线索

具身认知认为,概念形成和语言理解等高级心理过程本质上是以感知觉和运动经验为基础的。神经影像学研究发现,理解身体动作词激活了支配该部分肢体的感觉运动脑区。理解手部、脚部和面部动作词能够相应激活支配手部、脚部和面部的感觉运动脑区,体现出一种身体动作词语义理解激活的脑区与真实身体动作激活脑区的耦合效应。临床和经颅磁刺激研究结果表明,感觉运动皮层的激活与身体动作词语义处理具有因果性作用。未来研究应关注身体动作词语义理解的具身程度以及相关语言疗法在临床患者机能恢复中所起的作用。     

Adaptation to biological motion leads to a motion and a form aftereffect

Recent models have proposed a two-stage process of biological motion recognition. First, template or snapshot neurons estimate the body form. Then, motion is estimated from body form change. This predicts separate aftereffects for body form and body motion. We tested this prediction. Observers viewing leftward- or rightward-facing point-light walkers that walked forward or backward subsequently experienced oppositely directed aftereffects in stimuli ambiguous in the facing or the walking direction. These aftereffects did not originate from adaptation to the motion of the individual light points, because they occurred for limited-lifetime stimuli that restrict local motion. They also occurred when the adaptor displayed a random sequence of body postures that did not induce the walking motion percept. We thus conclude that biological motion gives rise to separate form and motion aftereffects and that body form representations are involved in biological motion perception.     

"But still, it moves"

A striking example of our sensitivity to dynamic information is our ability to infer motion from still images depicted in paintings, photographs or cartoons. What are the neural mechanisms that mediate this implied motion perception? In a recent paper, Krekelberg et al. demonstrate that form cues that imply motion are integrated with real motion information, and influence perception in both humans and monkeys and the neural processing in prototypical motion areas of the monkey brain.     

Categorical perception for voicing contrasts in normal and lead-treated rhesus monkeys: electrophysiological indices

Categorical perception of voicing contrasts was evaluated in rhesus monkeys. The monkeys had been chronically exposed to subclinical levels of lead either from conception to birth, or for approximately 6 months postnatally beginning at birth, or were never exposed to lead. Auditory evoked responses were recorded at 1 year of age from scalp electrodes placed over the left and right hemispheres during stimulus presentation. A late component of the brain responses recorded from the right temporal region of all monkeys discriminated between stimuli in a categorical manner. This pattern of responses was noted to be similar to that previously reported for humans. Categorical discriminations were also noted earlier in the waveforms for control monkeys and for monkeys exposed to lead prenatally, although this discrimination pattern shifted to the left hemisphere of the latter group. No such effects were noted for monkeys exposed to lead postnatally. These results suggest that the neurocortical mechanisms associated with categorical perception for voicing information may be similar across human and nonhuman primates. However, early exposure to lead appears to alter these processes.     

Techniques for the production of point-light and fully illuminated video displays from identical recordings

Illumination of only a few key points on a moving human body or face is enough to convey a compelling perception of human motion. A full understanding of the perception ofbiological motion from point-light displays requires accurate comparison with the perception of motion in normal, fully illuminated versions of the same images. Traditionally, these two types of stimuli (point-light and fully illuminated) have been filmed separately, allowing the introduction of uncontrolled variation across recordings. This is undesirable for accurate comparison of perceptual performance across the two types of display. This article describes simple techniques, using proprietary software, that allow production of point-light and fully illuminated video displays from identical recordings. These techniques are potentially useful for many studies of motion perception, by permitting precise comparison of perceptual performances across point-light displays and their fully illuminated counterparts with accuracy and comparative ease.     

Action Understanding in the Superior Temporal Sulcus Region

ABSTRACT— The posterior superior temporal sulcus (STS) region plays an important role in the perception of social acts, although its full role has not been completely clarified. This functional magnetic resonance imaging experiment examined activity in the STS region as participants viewed actions that were congruent or incongruent with intentions established by a previous emotional context. Participants viewed an actress express either a positive or a negative emotion toward one of two objects and then subsequently pick up one of them. If the object that was picked up had received positive regard, or if the object that was not picked up had received negative regard, the action was congruent; otherwise, the action was incongruent. Activity in the right posterior STS region was sensitive to the congruency between the action and the actress's emotional expression (i.e., STS activity was greater on incongruent than on congruent trials). These findings suggest that the posterior STS represents not only biological motion, but also how another person's motion is related to his or her intentions.     

The effect of experience and of dots’ density and duration on the detection of coherent motion in dogs

Knowledge about the mechanisms underlying canine vision is far from being exhaustive, especially that concerning post-retinal elaboration. One aspect that has received little attention is motion perception, and in spite of the common belief that dogs are extremely apt at detecting moving stimuli, there is no scientific support for such an assumption. In fact, we recently showed that dogs have higher thresholds than humans for coherent motion detection (Kanizsar et al. in Sci Rep UK 7:11259, 2017). This term refers to the ability of the visual system to perceive several units moving in the same direction, as one coherently moving global unit. Coherent motion perception is commonly investigated using random dot displays, containing variable proportions of coherently moving dots. Here, we investigated the relative contribution of local and global integration mechanisms for coherent motion perception, and changes in detection thresholds as a result of repeated exposure to the experimental stimuli. Dogs who had been involved in the previous study were given a conditioned discrimination task, in which we systematically manipulated dot density and duration and, eventually, re-assessed our subjects’ threshold after extensive exposure to the stimuli. Decreasing dot duration impacted on dogs’ accuracy in detecting coherent motion only at very low duration values, revealing the efficacy of local integration mechanisms. Density impacted on dogs’ accuracy in a linear fashion, indicating less efficient global integration. There was limited evidence of improvement in the re-assessment but, with an average threshold at re-assessment of 29%, dogs’ ability to detect coherent motion remains much poorer than that of humans.     

The Thatcher illusion in squirrel monkeys (Saimiri sciureus)

Like humans, Old World monkeys are known to use configural face processing to distinguish among individuals. The ability to recognize an individual through the perception of subtle differences in the configuration of facial features plays an important role in social cognition. To test this ability in New World monkeys, this study examined whether squirrel monkeys experience the Thatcher illusion, a measure of face processing ability in which changes in facial features are difficult to detect in an inverted face. In the experiment, the monkeys were required to distinguish between a target face and each of the three kinds of distracter faces whose features were altered to be different from those of the target. For each of the pairs of target and distracter faces, four rotation-based combinations of upright and inverted face presentations were used. The results revealed that when both faces were inverted and the eyes of the distracter face were altered by rotating them at an angle of 180° from those of the target face, the monkeys' discrimination learning was obstructed to a greater extent than it was under the other conditions. Thus, these results suggest that the squirrel monkey does experience the Thatcher illusion. Furthermore, it seems reasonable to assume that squirrel monkeys can utilize information about facial configurations in individual recognition and that this facial configuration information could be useful in their social communications.     

Auditory--visual cross-modal perception of communicative stimuli in tufted capuchin monkeys (Cebus apella)

Research on cross-modal performance in nonhuman primates is limited to a small number of sensory modalities and testing methods. To broaden the scope of this research, the authors tested capuchin monkeys (Cebus apella) for a seldom-studied cross-modal capacity in nonhuman primates, auditory-visual recognition. Monkeys were simultaneously played 2 video recordings of a face producing different vocalizations and a sound recording of 1 of the vocalizations. Stimulus sets varied from naturally occurring conspecific vocalizations to experimentally controlled human speech stimuli. The authors found that monkeys preferred to view face recordings that matched presented vocal stimuli. Their preference did not differ significantly across stimulus species or other stimulus features. However, the reliability of the latter set of results may have been limited by sample size. From these results, the authors concluded that capuchin monkeys exhibit auditory-visual cross-modal perception of conspecific vocalizations.     

Attentional modulation of visual motion perception

How is the perception and processing of visual motion affected by attention? This review examines recent research in cognition, perception and neurophysiology that explores how ongoing behavioural tasks (and the attentional states they impose) modulate the processing of visual motion. Although traditional views hold that motion is processed in an obligatory, 'pre-attentive' manner, evidence for processing in a task-independent manner is scant. Recent studies of human perception that have measured motion priming, motion aftereffects, uncertainty effects, and motion-interaction effects indicate instead that even simple aspects of motion processing may be substantially affected by whether motion information in a task is used or ignored by the perceiver. Single-unit studies in brain areas sensitive to visual motion in monkeys, and functional imaging studies on humans, also indicate that task and attentional state affect activity levels in brain regions thought to be important in motion perception. This review brings together these converging findings of attentional modulation of motion perception and considers them in light of object-oriented theories of attention.