Adding Years to Your Life (or at Least Looking Like It): A Simple Normalization Underlies Adaptation to Facial Age

Adaptation has been widely used to probe how experience shapes the visual encoding of faces, but the pattern of perceptual changes produced by adaptation and the neural mechanisms these imply remain poorly characterized. We explored how adaptation alters the perceived age of faces, a fundamental facial attribute which can uniquely and reliably be scaled by observers. This allowed us to measure how adaptation to one age level affected the full continuum of perceived ages. Participants guessed the ages of faces ranging from 18–89, before or after adapting to a different set of faces composed of younger, older, or middle-aged adults. Adapting to young or old faces induced opposite linear shifts in perceived age that were independent of the model''s age. Specifically, after adapting to younger or older faces, faces of all ages appeared 2 to 3 years older or younger, respectively. In contrast, middle-aged adaptors induced no aftereffects. This pattern suggests that adaptation leads to a simple and uniform renormalization of age perception, and is consistent with a norm-based neural code for the mechanisms mediating the perception of facial age.     

Low-level correlations between object properties and viewpoint can cause viewpoint-dependent object recognition

Viewpoint-dependent recognition performance of 3-D objects has often been taken as an indication of a viewpoint-dependent object representation. This viewpoint dependence is most often found using metrically manipulated objects. We aim to investigate whether instead these results can be explained by viewpoint and object property (e.g. curvature) information not being processed independently at a lower level, prior to object recognition itself. Multidimensional signal detection theory offers a useful framework, allowing us to model this as a low-level correlation between the internal noise distributions of viewpoint and object property dimensions. In Experiment 1, we measured these correlations using both Yes/No and adjustment tasks. We found a good correspondence across tasks, but large individual differences. In Experiment 2, we compared these results to the viewpoint dependence of object recognition through a Yes/No categorization task. We found that viewpoint-independent object recognition could not be fully reached using our stimuli, and that the pattern of viewpoint dependence was strongly correlated with the low-level correlations we measured earlier. In part, however, the viewpoint was abstracted despite these correlations. We conclude that low-level correlations do exist prior to object recognition, and can offer an explanation for some viewpoint effects on the discrimination of metrically manipulated 3-D objects.     

The hierarchy of directional interactions in visual motion processing

It is well known that context influences our perception of visual motion direction. For example, spatial and temporal context manipulations can be used to induce two well-known motion illusions: direction repulsion and the direction after-effect (DAE). Both result in inaccurate perception of direction when a moving pattern is either superimposed on (direction repulsion), or presented following adaptation to (DAE), another pattern moving in a different direction. Remarkable similarities in tuning characteristics suggest that common processes underlie the two illusions. What is not clear, however, is whether the processes driving the two illusions are expressions of the same or different neural substrates. Here we report two experiments demonstrating that direction repulsion and the DAE are, in fact, expressions of different neural substrates. Our strategy was to use each of the illusions to create a distorted perceptual representation upon which the mechanisms generating the other illusion could potentially operate. We found that the processes mediating direction repulsion did indeed access the distorted perceptual representation induced by the DAE. Conversely, the DAE was unaffected by direction repulsion. Thus parallels in perceptual phenomenology do not necessarily imply common neural substrates. Our results also demonstrate that the neural processes driving the DAE occur at an earlier stage of motion processing than those underlying direction repulsion.     

Dogs Evaluate Threatening Facial Expressions by Their Biological Validity – Evidence from Gazing Patterns

Appropriate response to companions’ emotional signals is important for all social creatures. The emotional expressions of humans and non-human animals have analogies in their form and function, suggesting shared evolutionary roots, but very little is known about how animals other than primates view and process facial expressions. In primates, threat-related facial expressions evoke exceptional viewing patterns compared with neutral or positive stimuli. Here, we explore if domestic dogs (Canis familiaris) have such an attentional bias toward threatening social stimuli and whether observed emotional expressions affect dogs’ gaze fixation distribution among the facial features (eyes, midface and mouth). We recorded the voluntary eye gaze of 31 domestic dogs during viewing of facial photographs of humans and dogs with three emotional expressions (threatening, pleasant and neutral). We found that dogs’ gaze fixations spread systematically among facial features. The distribution of fixations was altered by the seen expression, but eyes were the most probable targets of the first fixations and gathered longer looking durations than mouth regardless of the viewed expression. The examination of the inner facial features as a whole revealed more pronounced scanning differences among expressions. This suggests that dogs do not base their perception of facial expressions on the viewing of single structures, but the interpretation of the composition formed by eyes, midface and mouth. Dogs evaluated social threat rapidly and this evaluation led to attentional bias, which was dependent on the depicted species: threatening conspecifics’ faces evoked heightened attention but threatening human faces instead an avoidance response. We propose that threatening signals carrying differential biological validity are processed via distinctive neurocognitive pathways. Both of these mechanisms may have an adaptive significance for domestic dogs. The findings provide a novel perspective on understanding the processing of emotional expressions and sensitivity to social threat in non-primates.     

Activation of kinetically distinct synaptic conductances on inhibitory interneurons by electrotonically overlapping afferents

We measured brain activity during mental rotation and object recognition with objects rotated around three different axes. Activity in the superior parietal lobe (SPL) increased proportionally to viewpoint disparity during mental rotation, but not during object recognition. In contrast, the fusiform gyrus was preferentially recruited in a viewpoint-dependent manner in recognition as compared to mental rotation. In addition, independent of the effect of viewpoint, object recognition was associated with ventral areas and mental rotation with dorsal areas. These results indicate that the similar behavioral effects of viewpoint obtained in these two tasks are based on different neural substrates. Such findings call into question the hypothesis that mental rotation is used to compensate for changes in viewpoint during object recognition.     

Altered neuronal lineages in the facial ganglia of Hoxa2 mutant mice

Neurons of cranial sensory ganglia are derived from the neural crest and ectodermal placodes, but the mechanisms that control the relative contributions of each are not understood. Crest cells of the second branchial arch generate few facial ganglion neurons and no vestibuloacoustic ganglion neurons, but crest cells in other branchial arches generate many sensory neurons. Here we report that the facial ganglia of Hoxa2 mutant mice contain a large population of crest-derived neurons, suggesting that Hoxa2 normally represses the neurogenic potential of second arch crest cells. This may represent an anterior transformation of second arch neural crest cells toward a fate resembling that of first arch neural crest cells, which normally do not express Hoxa2 or any other Hox gene. We additionally found that overexpressing Hoxa2 in cultures of P19 embryonal carcinoma cells reduced the frequency of spontaneous neuronal differentiation, but only in the presence of cotransfected Pbx and Meis Hox cofactors. Finally, expression of Hoxa2 and the cofactors in chick neural crest cells populating the trigeminal ganglion also reduced the frequency of neurogenesis in the intact embryo. These data suggest an unanticipated role for Hox genes in controlling the neurogenic potential of at least some cranial neural crest cells.     

Spatially localized distortions of event time

A fundamental question about the perception of time is whether the neural mechanisms underlying temporal judgements are universal and centralized in the brain or modality specific and distributed. Time perception has traditionally been thought to be entirely dissociated from spatial vision. Here we show that the apparent duration of a dynamic stimulus can be manipulated in a local region of visual space by adapting to oscillatory motion or flicker. This implicates spatially localized temporal mechanisms in duration perception. We do not see concomitant changes in the time of onset or offset of the test patterns, demonstrating a direct local effect on duration perception rather than an indirect effect on the time course of neural processing. The effects of adaptation on duration perception can also be dissociated from motion or flicker perception per se. Although 20 Hz adaptation reduces both the apparent temporal frequency and duration of a 10 Hz test stimulus, 5 Hz adaptation increases apparent temporal frequency but has little effect on duration perception. We conclude that there is a peripheral, spatially localized, essentially visual component involved in sensing the duration of visual events.     

Viewer-centered object representation in the human visual system revealed by viewpoint aftereffects

Are there neurons representing specific views of objects in the human visual system? A visual selective adaptation method was used to address this question. After visual adaptation to an object viewed either 15 or 30 degrees from one side, when the same object was subsequently presented near the frontal view, the perceived viewing directions were biased in a direction opposite to that of the adapted viewpoint. This aftereffect can be obtained with spatially nonoverlapping adapting and test stimuli, and it depends on the global representation of the adapting stimuli. Viewpoint aftereffects were found within, but not across, categories of objects tested (faces, cars, wire-like objects). The magnitude of this aftereffect depends on the angular difference between the adapting and test viewing angles and grows with increasing duration of adaptation. These results support the existence of object-selective neurons tuned to specific viewing angles in the human visual system.     

Seeing fearful body expressions activates the fusiform cortex and amygdala

Darwin's evolutionary approach to organisms' emotional states attributes a prominent role to expressions of emotion in whole-body actions. Researchers in social psychology [1,2] and human development [3] have long emphasized the fact that emotional states are expressed through body movement, but cognitive neuroscientists have almost exclusively considered isolated facial expressions (for review, see [4]). Here we used high-field fMRI to determine the underlying neural mechanisms of perception of body expression of emotion. Subjects were presented with short blocks of body expressions of fear alternating with short blocks of emotionally neutral meaningful body gestures. All images had internal facial features blurred out to avoid confounds due to a face or facial expression. We show that exposure to body expressions of fear, as opposed to neutral body postures, activates the fusiform gyrus and the amygdala. The fact that these two areas have previously been associated with the processing of faces and facial expressions [5-8] suggests synergies between facial and body-action expressions of emotion. Our findings open a new area of investigation of the role of body expressions of emotion in adaptive behavior as well as the relation between processes of emotion recognition in the face and in the body.     

Slow and fast visual motion channels have independent binocular-rivalry stages

We have previously reported a transparent motion after-effect indicating that the human visual system comprises separate slow and fast motion channels. Here, we report that the presentation of a fast motion in one eye and a slow motion in the other eye does not result in binocular rivalry but in a clear percept of transparent motion. We call this new visual phenomenon 'dichoptic motion transparency' (DMT). So far only the DMT phenomenon and the two motion after-effects (the 'classical' motion after-effect, seen after motion adaptation on a static test pattern, and the dynamic motion after-effect, seen on a dynamic-noise test pattern) appear to isolate the channels completely. The speed ranges of the slow and fast channels overlap strongly and are observer dependent. A model is presented that links after-effect durations of an observer to the probability of rivalry or DMT as a function of dichoptic velocity combinations. Model results support the assumption of two highly independent channels showing only within-channel rivalry, and no rivalry or after-effect interactions between the channels. The finding of two independent motion vision channels, each with a separate rivalry stage and a private line to conscious perception, might be helpful in visualizing or analysing pathways to consciousness.     

Fluid Intelligence and Automatic Neural Processes in Facial Expression Perception: An Event-Related Potential Study

The relationship between human fluid intelligence and social-emotional abilities has been a topic of considerable interest. The current study investigated whether adolescents with different intellectual levels had different automatic neural processing of facial expressions. Two groups of adolescent males were enrolled: a high IQ group and an average IQ group. Age and parental socioeconomic status were matched between the two groups. Participants counted the numbers of the central cross changes while paired facial expressions were presented bilaterally in an oddball paradigm. There were two experimental conditions: a happy condition, in which neutral expressions were standard stimuli (p = 0.8) and happy expressions were deviant stimuli (p = 0.2), and a fearful condition, in which neutral expressions were standard stimuli (p = 0.8) and fearful expressions were deviant stimuli (p = 0.2). Participants were required to concentrate on the primary task of counting the central cross changes and to ignore the expressions to ensure that facial expression processing was automatic. Event-related potentials (ERPs) were obtained during the tasks. The visual mismatch negativity (vMMN) components were analyzed to index the automatic neural processing of facial expressions. For the early vMMN (50–130 ms), the high IQ group showed more negative vMMN amplitudes than the average IQ group in the happy condition. For the late vMMN (320–450 ms), the high IQ group had greater vMMN responses than the average IQ group over frontal and occipito-temporal areas in the fearful condition, and the average IQ group evoked larger vMMN amplitudes than the high IQ group over occipito-temporal areas in the happy condition. The present study elucidated the close relationships between fluid intelligence and pre-attentive change detection on social-emotional information.     

Network Adaptation Improves Temporal Representation of Naturalistic Stimuli in Drosophila Eye: II Mechanisms

Retinal networks must adapt constantly to best present the ever changing visual world to the brain. Here we test the hypothesis that adaptation is a result of different mechanisms at several synaptic connections within the network. In a companion paper (Part I), we showed that adaptation in the photoreceptors (R1–R6) and large monopolar cells (LMC) of the Drosophila eye improves sensitivity to under-represented signals in seconds by enhancing both the amplitude and frequency distribution of LMCs'' voltage responses to repeated naturalistic contrast series. In this paper, we show that such adaptation needs both the light-mediated conductance and feedback-mediated synaptic conductance. A faulty feedforward pathway in histamine receptor mutant flies speeds up the LMC output, mimicking extreme light adaptation. A faulty feedback pathway from L2 LMCs to photoreceptors slows down the LMC output, mimicking dark adaptation. These results underline the importance of network adaptation for efficient coding, and as a mechanism for selectively regulating the size and speed of signals in neurons. We suggest that concert action of many different mechanisms and neural connections are responsible for adaptation to visual stimuli. Further, our results demonstrate the need for detailed circuit reconstructions like that of the Drosophila lamina, to understand how networks process information.     

Dynamic large-scale connectivity of intrinsic cortical oscillations supports adaptive listening in challenging conditions

In multi-talker situations, individuals adapt behaviorally to this listening challenge mostly with ease, but how do brain neural networks shape this adaptation? We here establish a long-sought link between large-scale neural communications in electrophysiology and behavioral success in the control of attention in difficult listening situations. In an age-varying sample of N = 154 individuals, we find that connectivity between intrinsic neural oscillations extracted from source-reconstructed electroencephalography is regulated according to the listener’s goal during a challenging dual-talker task. These dynamics occur as spatially organized modulations in power-envelope correlations of alpha and low-beta neural oscillations during approximately 2-s intervals most critical for listening behavior relative to resting-state baseline. First, left frontoparietal low-beta connectivity (16 to 24 Hz) increased during anticipation and processing of a spatial-attention cue before speech presentation. Second, posterior alpha connectivity (7 to 11 Hz) decreased during comprehension of competing speech, particularly around target-word presentation. Connectivity dynamics of these networks were predictive of individual differences in the speed and accuracy of target-word identification, respectively, but proved unconfounded by changes in neural oscillatory activity strength. Successful adaptation to a listening challenge thus latches onto two distinct yet complementary neural systems: a beta-tuned frontoparietal network enabling the flexible adaptation to attentive listening state and an alpha-tuned posterior network supporting attention to speech.

This study investigates how intrinsic neural oscillations, acting in concert, tune into attentive listening. Using electroencephalography signals collected from people in a dual-talker listening task, the authors find that network connectivity of frontoparietal beta and posterior alpha oscillations is regulated according to the listener’s goal.     

Fractal rotation isolates mechanisms for form-dependent motion in human vision

Here, we describe a motion stimulus in which the quality of rotation is fractal. This makes its motion unavailable to the translation-based motion analysis known to underlie much of our motion perception. In contrast, normal rotation can be extracted through the aggregation of the outputs of translational mechanisms. Neural adaptation of these translation-based motion mechanisms is thought to drive the motion after-effect, a phenomenon in which prolonged viewing of motion in one direction leads to a percept of motion in the opposite direction. We measured the motion after-effects induced in static and moving stimuli by fractal rotation. The after-effects found were an order of magnitude smaller than those elicited by normal rotation. Our findings suggest that the analysis of fractal rotation involves different neural processes than those for standard translational motion. Given that the percept of motion elicited by fractal rotation is a clear example of motion derived from form analysis, we propose that the extraction of fractal rotation may reflect the operation of a general mechanism for inferring motion from changes in form.     

Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head

The vertebrate face contains bones that differentiate from mesenchymal cells of neural crest origin, which colonize the median nasofrontal bud and the first branchial arches. The patterning of individual facial bones and their relative positions occurs through mechanisms that remained elusive. During the early stages of head morphogenesis, an endodermal cul-de-sac, destined to become Sessel's pouch, underlies the nasofrontal bud. Reiterative outpocketings of the foregut then form the branchial pouches. We have tested the capacity of endoderm of the avian neurula to specify the facial skeleton by performing ablations or grafts of defined endodermal regions. Neural crest cells that do not express Hox genes respond to patterning cues produced regionally in the anterior endoderm to yield distinct skeletal components of the upper face and jaws. However, Hox-expressing neural crest cells do not respond to these cues. Bone orientation is likewise dependent on the position of the endoderm relative to the embryonic axes. Our findings thus indicate that the endoderm instructs neural crest cells as to the size, shape and position of all the facial skeletal elements, whether they are cartilage or membrane bones.     

Face and emotion expression processing and the serotonin transporter polymorphism 5‐HTTLPR/rs22531

Face cognition, including face identity and facial expression processing, is a crucial component of socio‐emotional abilities, characterizing humans as highest developed social beings. However, for these trait domains molecular genetic studies investigating gene–behavior associations based on well‐founded phenotype definitions are still rare. We examined the relationship between 5‐HTTLPR/rs25531 polymorphisms – related to serotonin‐reuptake – and the ability to perceive and recognize faces and emotional expressions in human faces. For this aim we conducted structural equation modeling on data from 230 young adults, obtained by using a comprehensive, multivariate task battery with maximal effort tasks. By additionally modeling fluid intelligence and immediate and delayed memory factors, we aimed to address the discriminant relationships of the 5‐HTTLPR/rs25531 polymorphisms with socio‐emotional abilities. We found a robust association between the 5‐HTTLPR/rs25531 polymorphism and facial emotion perception. Carriers of two long (L) alleles outperformed carriers of one or two S alleles. Weaker associations were present for face identity perception and memory for emotional facial expressions. There was no association between the 5‐HTTLPR/rs25531 polymorphism and non‐social abilities, demonstrating discriminant validity of the relationships. We discuss the implications and possible neural mechanisms underlying these novel findings.     

Transcranial Electrical Stimulation over Dorsolateral Prefrontal Cortex Modulates Processing of Social Cognitive and Affective Information

Recent neurofunctional studies suggested that lateral prefrontal cortex is a domain-general cognitive control area modulating computation of social information. Neuropsychological evidence reported dissociations between cognitive and affective components of social cognition. Here, we tested whether performance on social cognitive and affective tasks can be modulated by transcranial direct current stimulation (tDCS) over dorsolateral prefrontal cortex (DLPFC). To this aim, we compared the effects of tDCS on explicit recognition of emotional facial expressions (affective task), and on one cognitive task assessing the ability to adopt another person’s visual perspective. In a randomized, cross-over design, male and female healthy participants performed the two experimental tasks after bi-hemispheric tDCS (sham, left anodal/right cathodal, and right anodal/left cathodal) applied over DLPFC. Results showed that only in male participants explicit recognition of fearful facial expressions was significantly faster after anodal right/cathodal left stimulation with respect to anodal left/cathodal right and sham stimulations. In the visual perspective taking task, instead, anodal right/cathodal left stimulation negatively affected both male and female participants’ tendency to adopt another’s point of view. These findings demonstrated that concurrent facilitation of right and inhibition of left lateral prefrontal cortex can speed-up males’ responses to threatening faces whereas it interferes with the ability to adopt another’s viewpoint independently from gender. Thus, stimulation of cognitive control areas can lead to different effects on social cognitive skills depending on the affective vs. cognitive nature of the task, and on the gender-related differences in neural organization of emotion processing.     

A Major Controversy in Codon-Anticodon Adaptation Resolved by a New Codon Usage Index

Two alternative hypotheses attribute different benefits to codon-anticodon adaptation. The first assumes that protein production is rate limited by both initiation and elongation and that codon-anticodon adaptation would result in higher elongation efficiency and more efficient and accurate protein production, especially for highly expressed genes. The second claims that protein production is rate limited only by initiation efficiency but that improved codon adaptation and, consequently, increased elongation efficiency have the benefit of increasing ribosomal availability for global translation. To test these hypotheses, a recent study engineered a synthetic library of 154 genes, all encoding the same protein but differing in degrees of codon adaptation, to quantify the effect of differential codon adaptation on protein production in Escherichia coli. The surprising conclusion that “codon bias did not correlate with gene expression” and that “translation initiation, not elongation, is rate-limiting for gene expression” contradicts the conclusion reached by many other empirical studies. In this paper, I resolve the contradiction by reanalyzing the data from the 154 sequences. I demonstrate that translation elongation accounts for about 17% of total variation in protein production and that the previous conclusion is due to the use of a codon adaptation index (CAI) that does not account for the mutation bias in characterizing codon adaptation. The effect of translation elongation becomes undetectable only when translation initiation is unrealistically slow. A new index of translation elongation I_TE is formulated to facilitate studies on the efficiency and evolution of the translation machinery.     

Neural responses to facial and vocal expressions of fear and disgust.

Neuropsychological studies report more impaired responses to facial expressions of fear than disgust in people with amygdala lesions, and vice versa in people with Huntington''s disease. Experiments using functional magnetic resonance imaging (fMRI) have confirmed the role of the amygdala in the response to fearful faces and have implicated the anterior insula in the response to facial expressions of disgust. We used fMRI to extend these studies to the perception of fear and disgust from both facial and vocal expressions. Consistent with neuropsychological findings, both types of fearful stimuli activated the amygdala. Facial expressions of disgust activated the anterior insula and the caudate-putamen; vocal expressions of disgust did not significantly activate either of these regions. All four types of stimuli activated the superior temporal gyrus. Our findings therefore (i) support the differential localization of the neural substrates of fear and disgust; (ii) confirm the involvement of the amygdala in the emotion of fear, whether evoked by facial or vocal expressions; (iii) confirm the involvement of the anterior insula and the striatum in reactions to facial expressions of disgust; and (iv) suggest a possible general role for the perception of emotional expressions for the superior temporal gyrus.     

Network Adaptation Improves Temporal Representation of Naturalistic Stimuli in Drosophila Eye: I Dynamics

Because of the limited processing capacity of eyes, retinal networks must adapt constantly to best present the ever changing visual world to the brain. However, we still know little about how adaptation in retinal networks shapes neural encoding of changing information. To study this question, we recorded voltage responses from photoreceptors (R1–R6) and their output neurons (LMCs) in the Drosophila eye to repeated patterns of contrast values, collected from natural scenes. By analyzing the continuous photoreceptor-to-LMC transformations of these graded-potential neurons, we show that the efficiency of coding is dynamically improved by adaptation. In particular, adaptation enhances both the frequency and amplitude distribution of LMC output by improving sensitivity to under-represented signals within seconds. Moreover, the signal-to-noise ratio of LMC output increases in the same time scale. We suggest that these coding properties can be used to study network adaptation using the genetic tools in Drosophila, as shown in a companion paper (Part II).