Effects of unconscious processing on implicit memory for fearful faces

Emotional stimuli can be processed even when participants perceive them without conscious awareness, but the extent to which unconsciously processed emotional stimuli influence implicit memory after short and long delays is not fully understood. We addressed this issue by measuring a subliminal affective priming effect in Experiment 1 and a long-term priming effect in Experiment 2. In Experiment 1, a flashed fearful or neutral face masked by a scrambled face was presented three times, then a target face (either fearful or neutral) was presented and participants were asked to make a fearful/neutral judgment. We found that, relative to a neutral prime face (neutral-fear face), a fearful prime face speeded up participants' reaction to a fearful target (fear-fear face), when they were not aware of the masked prime face. But this response pattern did not apply to the neutral target. In Experiment 2, participants were first presented with a masked faces six times during encoding. Three minutes later, they were asked to make a fearful/neutral judgment for the same face with congruent expression, the same face with incongruent expression or a new face. Participants showed a significant priming effect for the fearful faces but not for the neutral faces, regardless of their awareness of the masked faces during encoding. These results provided evidence that unconsciously processed stimuli could enhance emotional memory after both short and long delays. It indicates that emotion can enhance memory processing whether the stimuli are encoded consciously or unconsciously.     

Action without awareness: reaching to an object you do not remember seeing

Background

Previous work by our group has shown that the scaling of reach trajectories to target size is independent of obligatory awareness of that target property and that “action without awareness” can persist for up to 2000 ms of visual delay. In the present investigation we sought to determine if the ability to scale reaching trajectories to target size following a delay is related to the pre-computing of movement parameters during initial stimulus presentation or the maintenance of a sensory (i.e., visual) representation for on-demand response parameterization.

Methodology/Principal Findings

Participants completed immediate or delayed (i.e., 2000 ms) perceptual reports and reaching responses to different sized targets under non-masked and masked target conditions. For the reaching task, the limb associated with a trial (i.e., left or right) was not specified until the time of response cuing: a manipulation that prevented participants from pre-computing the effector-related parameters of their response. In terms of the immediate and delayed perceptual tasks, target size was accurately reported during non-masked trials; however, for masked trials only a chance level of accuracy was observed. For the immediate and delayed reaching tasks, movement time as well as other temporal kinematic measures (e.g., times to peak acceleration, velocity and deceleration) increased in relation to decreasing target size across non-masked and masked trials.

Conclusions/Significance

Our results demonstrate that speed-accuracy relations were observed regardless of whether participants were aware (i.e., non-masked trials) or unaware (i.e., masked trials) of target size. Moreover, the equivalent scaling of immediate and delayed reaches during masked trials indicates that a persistent sensory-based representation supports the unconscious and metrical scaling of memory-guided reaching.     

Negative Affect Reduces Performance in Implicit Sequence Learning

Background

It is well documented that positive rather than negative moods encourage integrative processing of conscious information. However, the extent to which implicit or unconscious learning can be influenced by affective states remains unclear.

Methodology/Principal Findings

A Serial Reaction Time (SRT) task with sequence structures requiring integration over past trials was adopted to examine the effect of affective states on implicit learning. Music was used to induce and maintain positive and negative affective states. The present study showed that participants in negative rather than positive states learned less of the regularity. Moreover, the knowledge was shown by a Bayesian analysis to be largely unconscious as participants were poor at recognizing the regularity.

Conclusions/Significance

The results demonstrated that negative rather than positive affect inhibited implicit learning of complex structures. Our findings help to understand the effects of affective states on unconscious or implicit processing.     

Electrophysiological Differences in the Processing of Affect Misattribution

The affect misattribution procedure (AMP) was proposed as a technique to measure an implicit attitude to a prime image [1]. In the AMP, neutral symbols (e.g., a Chinese pictograph, called the target) are presented, following an emotional stimulus (known as the prime). Participants often misattribute the positive or negative affect of the priming images to the targets in spite of receiving an instruction to ignore the primes. The AMP effect has been investigated using behavioral measures; however, it is difficult to identify when the AMP effect occurs in emotional processing—whether the effect may occur in the earlier attention allocation stage or in the later evaluation stage. In this study, we examined the neural correlates of affect misattribution, using event-related potential (ERP) dividing the participants into two groups based on their tendency toward affect misattribution. The ERP results showed that the amplitude of P2 was larger for the prime at the parietal location in participants showing a low tendency to misattribution than for those showing a high tendency, while the effect of judging neutral targets amiss according to the primes was reflected in the late processing of targets (LPP). In addition, the topographic pattern analysis revealed that EPN-like component to targets was correlated with the difference of AMP tendency as well as P2 to primes and LPP to targets. Taken together, the mechanism of the affective misattribution was closely related to the attention allocation processing. Our findings provide neural evidence that evaluations of neutral targets are misattributed to emotional primes.     

Temporal-Spatial Neural Activation Patterns Linked to Perceptual Encoding of Emotional Salience

It is well known that we continuously filter incoming sensory information, selectively allocating attention to what is important while suppressing distracting or irrelevant information. Yet questions remain about spatiotemporal patterns of neural processes underlying attentional biases toward emotionally significant aspects of the world. One index of affectively biased attention is an emotional variant of an attentional blink (AB) paradigm, which reveals enhanced perceptual encoding for emotionally salient over neutral stimuli under conditions of limited executive attention. The present study took advantage of the high spatial and temporal resolution of magnetoencephalography (MEG) to investigate neural activation related to emotional and neutral targets in an AB task. MEG data were collected while participants performed a rapid stimulus visual presentation task in which two target stimuli were embedded in a stream of distractor words. The first target (T1) was a number and the second (T2) either an emotionally salient or neutral word. Behavioural results replicated previous findings of greater accuracy for emotionally salient than neutral T2 words. MEG source analyses showed that activation in orbitofrontal cortex, characterized by greater power in the theta and alpha bands, and dorsolateral prefrontal activation were associated with successful perceptual encoding of emotionally salient relative to neutral words. These effects were observed between 250 and 550 ms, latencies associated with discrimination of perceived from unperceived stimuli. These data suggest that important nodes of both emotional salience and frontoparietal executive systems are associated with the emotional modulation of the attentional blink.     

Can the meaning of multiple words be integrated unconsciously?

What are the limits of unconscious language processing? Can language circuits process simple grammatical constructions unconsciously and integrate the meaning of several unseen words? Using behavioural priming and electroencephalography (EEG), we studied a specific rule-based linguistic operation traditionally thought to require conscious cognitive control: the negation of valence. In a masked priming paradigm, two masked words were successively (Experiment 1) or simultaneously presented (Experiment 2), a modifier (‘not’/‘very’) and an adjective (e.g. ‘good’/‘bad’), followed by a visible target noun (e.g. ‘peace’/‘murder’). Subjects indicated whether the target noun had a positive or negative valence. The combination of these three words could either be contextually consistent (e.g. ‘very bad - murder’) or inconsistent (e.g. ‘not bad - murder’). EEG recordings revealed that grammatical negations could unfold partly unconsciously, as reflected in similar occipito-parietal N400 effects for conscious and unconscious three-word sequences forming inconsistent combinations. However, only conscious word sequences elicited P600 effects, later in time. Overall, these results suggest that multiple unconscious words can be rapidly integrated and that an unconscious negation can automatically ‘flip the sign’ of an unconscious adjective. These findings not only extend the limits of subliminal combinatorial language processes, but also highlight how consciousness modulates the grammatical integration of multiple words.     

Negativity Bias in Dangerous Drivers

The behavioral and cognitive characteristics of dangerous drivers differ significantly from those of safe drivers. However, differences in emotional information processing have seldom been investigated. Previous studies have revealed that drivers with higher anger/anxiety trait scores are more likely to be involved in crashes and that individuals with higher anger traits exhibit stronger negativity biases when processing emotions compared with control groups. However, researchers have not explored the relationship between emotional information processing and driving behavior. In this study, we examined the emotional information processing differences between dangerous drivers and safe drivers. Thirty-eight non-professional drivers were divided into two groups according to the penalty points that they had accrued for traffic violations: 15 drivers with 6 or more points were included in the dangerous driver group, and 23 drivers with 3 or fewer points were included in the safe driver group. The emotional Stroop task was used to measure negativity biases, and both behavioral and electroencephalograph data were recorded. The behavioral results revealed stronger negativity biases in the dangerous drivers than in the safe drivers. The bias score was correlated with self-reported dangerous driving behavior. Drivers with strong negativity biases reported having been involved in mores crashes compared with the less-biased drivers. The event-related potentials (ERPs) revealed that the dangerous drivers exhibited reduced P3 components when responding to negative stimuli, suggesting decreased inhibitory control of information that is task-irrelevant but emotionally salient. The influence of negativity bias provides one possible explanation of the effects of individual differences on dangerous driving behavior and traffic crashes.     

Infant pupil diameter changes in response to others' positive and negative emotions

It has been suggested that infants resonate emotionally to others' positive and negative affect displays, and that these responses become stronger towards emotions with negative valence around the age of 12-months. In this study we measured 6- and 12-month-old infants' changes in pupil diameter when presented with the image and sound of peers experiencing happiness, distress and an emotionally neutral state. For all participants the perception of another's distress triggered larger pupil diameters. Perceiving other's happiness also induced larger pupil diameters but for shorter time intervals. Importantly, we also found evidence for an asymmetry in autonomous arousal towards positive versus negative emotional displays. Larger pupil sizes for another's distress compared to another's happiness were recorded shortly after stimulus onset for the older infants, and in a later time window for the 6-month-olds. These findings suggest that arousal responses for negative as well as for positive emotions are present in the second half of the first postnatal year. Importantly, an asymmetry with stronger responses for negative emotions seems to be already present at this age.     

Cognitive set as a regulation factor in recognition of emotional facial expression

Effect of previous experience on the function of recognition of emotional facial expression was studied with the model of an unconscious visual set. It was found that repeated perception of pictures of face with angry expression caused a substantial effect on subsequent recognition of emotional facial expression. Recognition could be distorted, and expression of the face with "neutral" expression could be erroneously perceived as emotionally negative. Both contrast and assimilative illusions were observed. Evidence is presented that the described effect is the result of the set formation to emotional facial expression. The involvement of the prefrontal cortex into the structural-functional system of facial expression recognition is discussed. Kettel's test revealed significant correlations between the factor of rigidity of the set to emotional facial expression and the scores of personality traits such as social boldness--shyness on the H Scale, on the one hand, and the level of anxiety on the other.     

Are Age Effects in Positivity Influenced by the Valence of Distractors?

An age-related ‘positivity’ effect has been identified, in which older adults show an information-processing bias towards positive emotional items in attention and memory. In the present study, we examined this positivity bias by using a novel paradigm in which emotional and neutral distractors were presented along with emotionally valenced targets. Thirty-five older and 37 younger adults were asked during encoding to attend to emotional targets paired with distractors that were either neutral or opposite in valence to the target. Pupillary responses were recorded during initial encoding as well as a later incidental recognition task. Memory and pupillary responses for negative items were not affected by the valence of distractors, suggesting that positive distractors did not automatically attract older adults’ attention while they were encoding negative targets. Additionally, the pupil dilation to negative items mediated the relation between age and positivity in memory. Overall, memory and pupillary responses provide converging support for a cognitive control account of positivity effects in late adulthood and suggest a link between attentional processes and the memory positivity effect.     

Bilateral Skin Conductance Responses to Emotional Faces

Skin conductance responses (SCR) measure objective arousal in response to emotionally-relevant stimuli. Central nervous system influence on SCR is exerted differentially by the two hemispheres. Differences between SCR recordings from the left and right hands may therefore be expected. This study focused on emotionally expressive faces, known to be processed differently by the two hemispheres. Faces depicting neutral, happy, sad, angry, fearful or disgusted expressions were presented in two tasks, one with an explicit emotion judgment and the other with an age judgment. We found stronger responses to sad and happy faces compared with neutral from the left hand during the implicit task, and stronger responses to negative emotions compared with neutral from the right hand during the explicit task. Our results suggest that basic social stimuli generate distinct responses on the two hands, no doubt related to the lateralization of social function in the brain.     

Role of the Frontal Cortical Areas in the Analysis of Visual Stimuli at Conscious and Unconscious Levels

Event-related potentials (ERP) in response to complex target stimuli, which consisted of a central recognizable picture and a lateral masked image (analyzed at the unconscious level) were recorded in adult subjects and seven-year-old children. ERP components N200, N300, and P400/N400 had different topography and were differently pronounced in adults and children. In adult subjects, the N200 component that reflects the processing of a sensory stimulus was recorded in the temporo-parieto-occipital and occipital areas. In children, N200 was recorded in the caudal regions and the frontal areas of the cortex. Analysis of different waveforms obtained by subtraction of the ERP to the central stimulus from the ERP to the complex stimulus showed that unconscious stimulus processing in adult subjects is not reflected in the ERP structure. In children, an unconsciously processed image incorporated into a complex stimulus evokes processing negativity in the occipital and frontal cortical areas. Comparison of ERP in groups of children divided by their reflectivity/impulsivity showed that, predominantly, the left frontal area is involved in image analysis at the unconscious level in reflective children and, predominantly, the right frontal area participates in unconscious image analysis in impulsive children. It is suggested that the perfection of the visual recognition of a target stimulus, which contains additional unconsciously processed information, consists in growth of the involvement of the left-hemispheric mechanisms (with respective growth of significance of the left-hemispheric mechanisms) and in a decrease in the role of the frontal areas in analysis of sensory information.     

Visuospatial Sequence Learning without Seeing

Background

The ability to detect and integrate associations between unrelated items that are close in space and time is a key feature of human learning and memory. Learning sequential associations between non-adjacent visual stimuli (higher-order visuospatial dependencies) can occur either with or without awareness (explicit vs. implicit learning) of the products of learning. Existing behavioural and neurocognitive studies of explicit and implicit sequence learning, however, are based on conscious access to the sequence of target locations and, typically, on conditions where the locations for orienting, or motor, responses coincide with the locations of the target sequence.

Methodology/Principal Findings

Dichoptic stimuli were presented on a novel sequence learning task using a mirror stereoscope to mask the eye-of-origin of visual input from conscious awareness. We demonstrate that conscious access to the sequence of target locations and responses that coincide with structure of the target sequence are dispensable features when learning higher-order visuospatial associations. Sequence knowledge was expressed in the ability of participants to identify the trained higher-order visuospatial sequence on a recognition test, even though the trained and untrained recognition sequences were identical when viewed at a conscious binocular level, and differed only at the level of the masked sequential associations.

Conclusions/Significance

These results demonstrate that unconscious processing can support perceptual learning of higher-order sequential associations through interocular integration of retinotopic-based codes stemming from monocular eye-of-origin information. Furthermore, unlike other forms of perceptual associative learning, visuospatial attention did not need to be directed to the locations of the target sequence. More generally, the results pose a challenge to neural models of learning to account for a previously unknown capacity of the human visual system to support the detection, learning and recognition of higher-order sequential associations under conditions where observers are unable to see the target sequence or perform responses that coincide with structure of the target sequence.     

Environmental and genetic effects shape the development of personality traits in the mangrove killifish Kryptolebias marmoratus

Consistent individual differences in behaviour are well documented, for example, individuals can be defined as consistently bold or consistently shy. To date our understanding of the mechanisms underpinning consistent individual differences in behaviour (also termed behavioural types (BTs)) remains limited. Theoretical work suggests life‐history tradeoffs drive BT variation, however, empirical support is scarce. Moreover, whilst life‐history is known to be phenotypically plastic in response to environmental conditions during ontogeny, the extent to which such plasticity drives plasticity in behavioural traits and personality remains poorly understood. Using a natural clonal vertebrate, Kryptolebias marmoratus, we control for genetic variation and investigate developmental plasticity in life‐history and three commonly studied behavioural traits (exploration, boldness, aggression) in response to three ecologically relevant environments; conspecific presence, low food and perceived risk. Simulated predation risk was the only treatment that generated repeatable behaviour i.e. personality during ontogeny. Treatments differed in their effects on mean life‐history and behavioural scores. Specifically, low food fish exhibited reduced growth rate and exploration but did not differ from control fish in their boldness or aggression scores. Conspecific presence resulted in a strong negative effect on mean aggression, boldness and exploration during ontogeny but had minimal effect on life‐history traits. Simulated predation risk resulted in increased reproductive output but had minimal effect upon average behavioural scores. Together these results suggest that life‐history plasticity/variation may be insufficient in driving variation in personality during development. Finally, using offspring derived from each rearing environment we investigate maternal effects and find strong maternal influence upon offspring size, but not behaviour. These results highlight and support the current understanding that risk perception is important in shaping personality, and that social experience during ontogeny is a major influence upon behavioural expression.     

The flexible nature of unconscious cognition

The cognitive signature of unconscious processes is hotly debated recently. Generally, consciousness is thought to mediate flexible, adaptive and goal-directed behavior, but in the last decade unconscious processing has rapidly gained ground on traditional conscious territory. In this study we demonstrate that the scope and impact of unconscious information on behavior and brain activity can be modulated dynamically on a trial-by-trial basis. Participants performed a Go/No-Go experiment in which an unconscious (masked) stimulus preceding a conscious target could be associated with either a Go or No-Go response. Importantly, the mapping of stimuli onto these actions varied on a trial-by-trial basis, preventing the formation of stable associations and hence the possibility that unconscious stimuli automatically activate these control actions. By eliminating stimulus-response associations established through practice we demonstrate that unconscious information can be processed in a flexible and adaptive manner. In this experiment we show that the same unconscious stimulus can have a substantially different effect on behavior and (prefrontal) brain activity depending on the rapidly changing task context in which it is presented. This work suggests that unconscious information processing shares many sophisticated characteristics (including flexibility and context-specificity) with its conscious counterpart.     

Effect of Subliminal Lexical Priming on the Subjective Perception of Images: A Machine Learning Approach

The purpose of the study is to examine the effect of subliminal priming in terms of the perception of images influenced by words with positive, negative, and neutral emotional content, through electroencephalograms (EEGs). Participants were instructed to rate how much they like the stimuli images, on a 7-point Likert scale, after being subliminally exposed to masked lexical prime words that exhibit positive, negative, and neutral connotations with respect to the images. Simultaneously, the EEGs were recorded. Statistical tests such as repeated measures ANOVAs and two-tailed paired-samples t-tests were performed to measure significant differences in the likability ratings among the three prime affect types; the results showed a strong shift in the likeness judgment for the images in the positively primed condition compared to the other two. The acquired EEGs were examined to assess the difference in brain activity associated with the three different conditions. The consistent results obtained confirmed the overall priming effect on participants’ explicit ratings. In addition, machine learning algorithms such as support vector machines (SVMs), and AdaBoost classifiers were applied to infer the prime affect type from the ERPs. The highest classification rates of 95.0% and 70.0% obtained respectively for average-trial binary classifier and average-trial multi-class further emphasize that the ERPs encode information about the different kinds of primes.     

The Effect of Emotional Distance on Psychophysiologic Concordance and Perceived Empathy Between Patient and Interviewer

– This preliminary study investigated the effect of emotional distance on psychophysiologic concordance and perceived empathy in a clinical population. Participants included 20 adult outpatients from a mental health clinic that underwent a brief semi-structured interview with a trained psychiatrist in either an emotionally neutral or an emotionally distant condition. Simultaneous skin conductance (SC) levels of the patient and interviewer were recorded and used to calculate a measure of psychophysiologic concordance. Interviewer gaze was rated by an independent observer and used as a proxy indicator of emotional distance. Observer ratings of interviewer gaze, SC concordance, and patient ratings of perceived interviewer empathy were significantly lower in the emotionally distant condition compared with the emotionally neutral condition (p < 0.05). Results suggest that increased emotional distance is associated with decreased psychophysiologic concordance and reduced subjective ratings of perceived empathy. The observed differences in psychophysiologic concordance support the use of this measure as a potential marker of empathy in a clinical population in an interview setting.     

Dynamics of heart rhythm in chimpanzees during the perception of the emotionally colored human voice

The performed study allowed to observe in two chimpanzees both common and individual changes of the heart rate under the action of human voice with emotionally positive or negative intonation, as well as under the action of preferred (sweet) or rejected (quinine solution) natural stimulus. The common property consists in a significant slowing down of the heart rate in response to negative vocal signal and rejected natural stimulus and in only slight change of the heart rate in response to positive signals. Individual properties comprise differences in reactions of the cardiovascular system of both animals to negative action: a greater efficiency of the vocal signal for one chimpanzee and of the direct (natural) stimulus for the second one.     

On the blink: the importance of target-distractor similarity in eliciting an attentional blink with faces

Temporal allocation of attention is often investigated with a paradigm in which two relevant target items are presented in a rapid sequence of irrelevant distractors. The term Attentional Blink (AB) denotes a transient impairment of awareness for the second of these two target items when presented close in time. Experimental studies reported that the AB is reduced when the second target is emotionally significant, suggesting a modulation of attention allocation. The aim of the present study was to systematically investigate the influence of target-distractor similarity on AB magnitude for faces with emotional expressions under conditions of limited attention in a series of six rapid serial visual presentation experiments. The task on the first target was either to discriminate the gender of a neutral face (Experiments 1, 3-6) or an indoor/outdoor visual scene (Experiment 2). The task on the second target required either the detection of emotional expressions (Experiments 1-5) or the detection of a face (Experiment 6). The AB was minimal or absent when targets could be easily discriminated from each other. Three successive experiments revealed that insufficient masking and target-distractor similarity could account for the observed immunity of faces against the AB in the first two experiments. An AB was present but not increased when the facial expression was irrelevant to the task suggesting that target-distractor similarity plays a more important role in eliciting an AB than the attentional set demanded by the specific task. In line with previous work, emotional faces were less affected by the AB.     

Effect of acute and chronic deprivation of catecholaminergic system activity induced by 6-hydroxydopamine on the behavior of the rat

On 202 male rats of Wistar line, a study was carried out of the effect of chronic and acute deprivations of the brain CA-systems activity resulting from administration of 6-OHDA on investigating behaviour and learning. Chronic deprivation of CA-systems activity by neonatal administration of 6-OHDA (100 mg/kg subcutaneously) and their acute deprivation by intracerebral administration of 6-OHDA to adult rats (150 mkg in each lateral ventriculus) was accompanied by similar deep changes of behaviour. Both forms of deprivation reduced the investigating activity of the animals in the open field. In both cases, the above 6-OHDA dozes sharply impeded the learning of animals with emotionally negative reinforcement, with no significant influence on learning with emotionally positive reinforcement. Both forms of deprivation of CA-systems activity weakened the reaction of frustration elicited by a sharp reduction of food reinforcement.