Sustained activation and executive control in the avian prefrontal cortex

We review our studies examining neural correlates of directed forgetting and executive control in the avian prefrontal cortex. One of the fundamental forms of executive control is the ability to selectively filter information, retaining that which is critical for the current purposes and discarding that which is not. In our first experiment, we trained birds on a directed-forgetting version of a delayed matching-to-sample task. Following a sample stimulus, a bird heard either a remember tone indicating that a memory test would follow, or a forget tone indicating that no memory test would be given. We found that neural activity in the avian prefrontal cortex increased when the bird was told to remember, and decreased when the bird was told to forget. Behavioral probe tests confirmed that the animals were forgetting on forget trials.Although the sustained activation observed on remember trials and the absence of such activation on forget trials could be a code of remembering and forgetting the sample stimulus, it could also be a code of the possibility of obtaining a reward. To address this issue we conducted a second study in which we used three cues: remember, forget, and forget–reward. The forget–reward cue instructed the subject to forget the sample yet at the same time provided a free reward. Neural activity on forget–reward trials matched that on remember trials tentatively indicating that the sustained activation on remember trials might be a reward code rather than a sample stimulus code. Behavioral probe tests, however, failed to indicate that the animals were forgetting on forget–reward trials, and hence it still is possible that the sustained activation could be a code for memory of the sample stimulus.     

Predictive validity of event-related potentials (ERPs) in relation to the directed forgetting effects.

OBJECTIVE: A directed forgetting paradigm (word method) was used to assess the relationships between the event-related potentials (ERPs) recorded during the study phase and the subsequent forgetting effects. METHODS: In the study phase 100 words were presented each followed by either an instruction to remember (R) or to forget (F). Then these 100 words, together with another 100 new words, were presented and subjects had to perform an old/new decision task. The forgetting effect was considered as the difference between the rate of R- and F-words correctly recognised. Based on this difference, the whole sample was divided into two 10-subject groups with high and low forgetting effect. RESULTS: From 300 to 600 msec post-instruction differences in ERPs between R and F instructions were similar in both groups. In contrast, in the 100-300 msec epoch, ERP differences only appeared in the high-effect group and consisted of an enhanced positive activity elicited by F instruction at frontal and prefrontal areas and a larger positivity associated to R instruction at parietal area. CONCLUSIONS: The findings suggest that the processing of the word is kept on stand-by until the instruction is provided. Instruction to remember would reactivate this processing, which would mainly involve the parietal area, whereas instruction to forget appears to trigger frontal and prefrontal mechanisms trying to inhibit such processing.     

Culture shapes electrocortical responses during emotion suppression

Previous work has shown that emotional control is highly valued in Asian culture. However, little is known about how this cultural value might influence emotional processing. Here, we hypothesized that Asians are ‘culturally trained’ to down-regulate emotional processing when required to suppress emotional expressions. Such down-regulation, however, is unlikely for European Americans because their culture values emotional expression (vs control) more. To test these predictions, we adopted the parietal late positive potential (LPP) of the event-related potential as an objective indicator of emotional processing. Both Asian and European Americans were exposed to either unpleasant or neutral pictures while instructed to either attend or suppress expression of emotions. Both groups showed an equally pronounced parietal positivity ∼600 ms post-stimulus. As predicted, however, Asians subsequently showed a significant decrease of the parietal LPP in the suppression (vs attend) condition. The initial positivity completely disappeared 2000 ms post-stimulus. In contrast, for European Americans the parietal LPP suppression effect was completely absent although there was an early occurring, sustained increase in frontal positivity in the suppression (vs attend) condition. Implications for culture and emotion research are discussed.     

An electrophysiological test of directed forgetting: the role of retrieval inhibition

A central issue in the research of directed forgetting is whether the differential memory performance for to-be-remembered (TBR) and to-be-forgotten (TBF) items is solely due to differential encoding or whether retrieval inhibition of TBF items plays an additional role. In this study, recognition-related event-related brain potentials (ERPs) were used to examine this issue. The spatio-temporal distributions of the old/new ERP effects obtained in Experiment 1 that employed a directed forgetting paradigm were compared with those recorded in Experiment 2 in which the level of processing was manipulated. In Experiment 1, participants were instructed to remember or to forget words by means of a cue presented after each word. ERPs recorded in the recognition test revealed early phasic frontal and parietal old/new effects for TBR items, whereas TBF items elicited only a frontal old/new effect. Moreover, a late right-frontal positive slow wave was more pronounced for TBF items, suggesting that those items were associated with a larger amount of post-retrieval processing. In Experiment 2, the same cueing method and the same stimulus materials were used, and memory encoding was manipulated by cueing participants to process the words either deeply or shallowly. Both deeply and shallowly encoded items elicited phasic frontal and parietal old/new effects followed by a late right-frontal positive slow wave. However, in contrast to TBR and TBF items, these effects differed only quantitatively. The results suggest that differential encoding alone cannot account for the effects of directed forgetting. They are more consistent with the view that items followed by an instruction to forget become inhibited and less accessible, and, therefore, more difficult to retrieve.     

Motivated and controlled attention to emotion: Time-course of the late positive potential

ObjectiveThe present study examined the time-course of automatic and controlled modulation of the late positive potential (LPP) during emotional picture viewing.MethodsParticipants (N = 32) viewed neutral and unpleasant stimuli for 6000 ms; at 3000 ms, one of two tones signaled participants to attend either to a more or less arousing portion of the picture. The time-course of the LPP was examined both during the passive viewing and directed attention portions of the trial using the method proposed by Guthrie and Buchwald [Guthrie D, Buchwald JS. Significance testing of difference potentials. Psychophysiology 1991;28(2):240–4].ResultsDuring passive viewing, the LPP became reliably larger following the presentation of unpleasant pictures from 160 ms onward; the magnitude of the LPP became reliably smaller beginning 620 ms after participants were instructed to attend to the less arousing aspects of unpleasant pictures – and this difference was maintained throughout the duration of the trial.ConclusionsThe LPP reflects relatively automatic attention to emotional visual stimuli, but is also sensitive to manipulations of directed attention toward arousing versus neutral aspects of such stimuli.SignificanceThese results shed further light on the time-course of emotional and cognitive modulation of the LPP, and suggest that the LPP reflects the relatively rapid and dynamic allocation of increased attention to emotional stimuli.     

Brain dynamics of visual attention during anticipation and encoding of threat- and safe-cues in spider-phobic individuals

This study systematically investigated the sensitivity of the phobic attention system by measuring event-related potentials (ERPs) in spider-phobic and non-phobic volunteers in a context where spider and neutral pictures were presented (phobic threat condition) and in contexts where no phobic but unpleasant and neutral or only neutral pictures were displayed (phobia-irrelevant conditions). In a between-group study, participants were assigned to phobia-irrelevant conditions either before or after the exposure to spider pictures (pre-exposure vs post-exposure participants). Additionally, each picture was preceded by a fixation cross presented in one of three different colors that were informative about the category of an upcoming picture. In the phobic threat condition, spider-phobic participants showed a larger P1 than controls for all pictures and signal cues. Moreover, individuals with spider phobia who were sensitized by the exposure to phobic stimuli (i.e. post-exposure participants) responded with an increased P1 also in phobia-irrelevant conditions. In contrast, no group differences between spider-phobic and non-phobic individuals were observed in the P1-amplitudes during viewing of phobia-irrelevant stimuli in the pre-exposure group. In addition, cues signaling neutral pictures elicited decreased stimulus-preceding negativity (SPN) compared with cues signaling emotional pictures. Moreover, emotional pictures and cues signaling emotional pictures evoked larger early posterior negativity (EPN) and late positive potential (LPP) than neutral stimuli. Spider phobics showed greater selective attention effects than controls for phobia-relevant pictures (increased EPN and LPP) and cues (increased LPP and SPN). Increased sensitization of the attention system observed in spider-phobic individuals might facilitate fear conditioning and promote generalization of fear playing an important role in the maintenance of anxiety disorders.     

The role of the medial frontal cortex in the maintenance of emotional states

Evidence is accruing that people can maintain their emotional states, but how they do it and which brain regions are responsible still remains unclear. We examined whether people maintain emotional states ‘actively’, with explicit elaboration of the emotion, or ‘passively’, without elaboration. Twenty-four participants completed an emotion maintenance task in which they either maintained the emotional intensity from the first picture of a pair to compare to that of the second picture (‘maintain’ condition), or only rated their emotional response to the second picture (‘non-maintain’ condition). Supporting the ‘active’ maintenance hypothesis, when maintaining vs not maintaining emotion, participants exhibited increased height and width of activation in the dorsal medial frontal cortex (MFC) and lateral prefrontal cortex, regions associated with explicit emotion generation and manipulation of contents in working memory, respectively. Supporting the ‘passive’ maintenance hypothesis, however, when viewing negative emotional pictures (vs neutral pictures) that were not explicitly maintained, participants exhibited greater duration of activity in the rostral MFC, a region associated with implicit emotion generation. Supported by behavioral findings, this evidence that people maintain emotional states both naturally in the rMFC and strategically in the dMFC may be critical for understanding normal as well as disordered emotion regulation.     

Electrocortical evidence of increased post-reappraisal neural reactivity and its link to depressive symptoms

Few studies have examined whether effortful emotion regulation has a protracted impact on subsequent affective appraisal, and even fewer have investigated this effect on a trial-by-trial basis. In this study, we hypothesized that engaging cognitive resources via reappraisal during a trial would result in a subsequent period of increased reactivity on the next trial, as quantified using event-related potentials and oscillations. Forty-eight healthy individuals passively viewed unpleasant and neutral pictures followed by an auditory instruction to either continue viewing normally or reappraise emotional response to pictures. Viewing unpleasant pictures yielded increased late positive potential (LPP) and decreased posterior alpha (8–13 Hz) compared with neutral pictures. A similar pattern was observed on trials that immediately ‘followed’ emotion regulation instructions. Moreover, individuals with increased self-reported depressive symptoms showed greater LPP and alpha modulation following emotion regulation, suggesting that these responses may relate to compromised emotion regulation ability. This study demonstrates that cognitive reappraisal induces subsequent heightened reactivity that may reflect transient resource depletion, and these effects are more pronounced among those with increased depressive symptoms. Interventions that focus on emotion regulation might use these electrocortical markers to track changes in regulatory efficacy.     

Suppression of aversive memories associates with changes in early and late stages of neurocognitive processing

Unwanted memories, such as emotionally negative, can be intentionally suppressed through voluntary control in humans. Memory suppression is thought to be mediated by the interplay of a chain of neurocognitive processes. However, empirical data in support of this notion is lacking. Using high-temporal resolution event-related potential (ERP) technique, we investigated the time course of ERPs associated with suppression of negative and neutral memories in a Think/No-Think paradigm in young, healthy participants. Results showed that participants had greater difficulty in suppressing emotionally negative memories than neutral ones. ERPs and source analyses demonstrated that memory suppression processing for negative and neutral memories were generally associated with changes during early components of a time window of 70-260ms, such as P1 and N2, mainly at the right inferior frontal gyrus and occipital lobe; suppression of aversive memories was associated with two major late ERP components between 380 and 800ms, with significantly smaller later negativity (LN) but larger late parietal positivity (LPP), primarily at the right medial and superior frontal gyri. These results suggest that differences in early components may reflect early stages of suppression processing including visual awareness, attention reallocation, and executive processing. Differences in late components between suppression of aversive and neutral memories may reflect a process of down-regulating conscious recollection of memory representations supported by prefrontal and parietal networks. A less effective control of this process, as evidenced by smaller LN and larger LPP, may explain the fact that emotionally negative memories were harder to be suppressed. Altogether, these findings suggest that suppression of aversive memories requires down-regulation of late conscious recollection, which can be dissociated from early visual and attention processing in memory suppression.     

Absence of a positive bias in social anxiety: the application of a directed forgetting paradigm

The present study used a directed forgetting paradigm to investigate whether socially anxious individuals show a memory bias for social information. Socially anxious and non-anxious participants viewed three types of words: socially negative, socially positive, and neutral. Each word was presented on a computer screen and was followed by a cue instructing participants to either remember or forget the word. A free recall test and a recognition test were then administered by asking participants to recall and recognize both “to-be-remembered” and “to-be-forgotten” words. When compared to non-anxious participants, socially anxious participants showed a greater directed forgetting effect for socially positive words in the free recall test, indicating that socially anxious individuals more easily forget socially positive words than do non-anxious individuals. This result suggests that socially anxious individuals lack the positive bias (i.e., difficulty in forgetting socially positive information) displayed by non-anxious individuals.     

Age-related differences in event-related potentials for early visual processing of emotional faces

With advancing age, processing resources are shifted away from negative emotional stimuli and toward positive ones. Here, we explored this ‘positivity effect’ using event-related potentials (ERPs). Participants identified the presence or absence of a visual probe that appeared over photographs of emotional faces. The ERPs elicited by the onsets of angry, sad, happy and neutral faces were recorded. We examined the frontocentral emotional positivity (FcEP), which is defined as a positive deflection in the waveforms elicited by emotional expressions relative to neutral faces early on in the time course of the ERP. The FcEP is thought to reflect enhanced early processing of emotional expressions. The results show that within the first 130 ms young adults show an FcEP to negative emotional expressions, whereas older adults show an FcEP to positive emotional expressions. These findings provide additional evidence that the age-related positivity effect in emotion processing can be traced to automatic processes that are evident very early in the processing of emotional facial expressions.     

Are there sex differences in ERPs related to processing empathy-evoking pictures?

ObjectiveThis study aimed to investigate sex differences in the temporal dynamics of experiencing empathy by using electrophysiological measurements.MethodsTwenty-five females and 27 males viewed 414 pictures of the International affective picture system varying in emotional valence (positive, negative and neutral) and presence of humans (human and scenes). EEG event related potentials (ERPs) were obtained and correlations were computed with self-reported empathy.ResultsCompared to males, females showed increased anterior N2 and parietal LPP amplitudes to humans contrasted with scenes (independent of emotional valence) and to negative contrasted with neutral emotions (independent of human presence). Independent of sex the N1 and anterior N2 were specifically increased for positive human emotions and the parietal LPP for negative human emotions. Across sexes, the N2 and LPP human emotion effects and LPP human effects were associated with self-reported affective empathy, but not with cognitive empathy.ConclusionsThis study provides electrophysiological evidence that women prioritize the processing of socially relevant and negative emotional information, but that women did not show enhanced brain potentials to pictures with positive or negative emotions in humans.     

‘Ecstasy’ as a social drug: MDMA preferentially affects responses to emotional stimuli with social content

3,4-Methylenedioxymethamphetamine (MDMA, ‘ecstasy’) is used recreationally to improve mood and sociability, and has generated clinical interest as a possible adjunct to psychotherapy. One way that MDMA may produce positive ‘prosocial’ effects is by changing responses to emotional stimuli, especially stimuli with social content. Here, we examined for the first time how MDMA affects subjective responses to positive, negative and neutral emotional pictures with and without social content. We hypothesized that MDMA would dose-dependently increase reactivity to positive emotional stimuli and dampen reactivity to negative stimuli, and that these effects would be most pronounced for pictures with people in them. The data were obtained from two studies using similar designs with healthy occasional MDMA users (total N = 101). During each session, participants received MDMA (0, 0.75 and 1.5 mg/kg oral), and then rated their positive and negative responses to standardized positive, negative and neutral pictures with and without social content. MDMA increased positive ratings of positive social pictures, but reduced positive ratings of non-social positive pictures. We speculate this ‘socially selective’ effect contributes to the prosocial effects of MDMA by increasing the comparative value of social contact and closeness with others. This effect may also contribute to its attractiveness to recreational users.     

Heritability of the neural response to emotional pictures: evidence from ERPs in an adult twin sample

Affect-modulated event-related potentials (ERPs) are increasingly used to study psychopathology and individual differences in emotion processing. Many have suggested that variation in these neural responses reflects genetically mediated risk. However, to date, no studies have demonstrated genetic contributions to affect-modulated ERPs. The present study therefore sought to examine the heritability of a range of ERPs elicited during affective picture viewing. One hundred and thirty monozygotic and 124 dizygotic twin pairs passively viewed 30 pleasant, 30 neutral and 30 unpleasant images for 6 s each. The early posterior negativity was scored for each subject; in addition, the P300/late positive potential (LPP) was scored in multiple time windows and sites. Results indicate that the centro-parietal P300 (occurring between 300 and 600 ms) is subject to substantial genetic contributions. Furthermore, variance in the P300 elicited by affective stimuli was moderately heritable even after controlling for the P300 elicited by neutral stimuli. Later and more frontal activation (i.e. between 1000 and 3000 ms) also showed evidence of heritablity. Early parietal, and perhaps later frontal portions of the P300/LPP complex, may therefore represent promising neurobehavioral markers of genetically influenced processing of emotional information.     

Avoidant encoding in acute stress disorder: a prospective study

This study investigated the relationship between ongoing posttraumatic adjustment and encoding style. Eleven acute stress disorder (ASD) participants and 14 non-traumatized controls completed the item method of directed forgetting and were retested 1 year later. Trauma-related, positive and neutral words were followed by a "remember" or "forget" instruction. At Time 1, ASD participants demonstrated directed forgetting for trauma and neutral words; controls showed directed forgetting for all word types. At Time 2, directed forgetting was replicated in controls for each word type, but only for neutral words in the ASD group. Directed forgetting effects were absent for positive words in the ASD group. The findings raise the possibility that individuals who develop ASD possess an encoding style for positive material that reflects a trait-like manner of information processing.     

Prefrontal-occipitoparietal coupling underlies late latency human neuronal responses to emotion

Enhanced late positive potentials (LPPs) evoked by highly arousing unpleasant and pleasant stimuli have been consistently observed in event-related potential experiments in humans. Although the psychological factors modulating the LPP have been studied in detail, the neurobiological underpinnings of this response remain poorly understood. Current models suggest that the LPP is a product of both an automatic facilitation of perceptual activity, as well as postperceptual processing under cognitive control. Here we applied magnetoencephalography (MEG) and beamformer analysis combined with Granger causality measures to provide a mechanistic account for LPP generation that reconciles these two models. We demonstrate that the magnetic homolog of the LPP, mLPP, is localized within bilateral occipitoparietal and right prefrontal cortex. Critically, directed functional connectivity analysis between these brain regions, indexed by Granger causality, demonstrates stronger bidirectional influences between frontal and occipitoparietal cortex for high arousing emotional relative to low arousing neutral pictures. Thus, both bottom-up and top-down accounts of the late latency response to emotion derived from psychological studies can be explained by a reciprocal codependency between activity in prefrontal and occipitoparietal cortex.     

Repetitive picture processing: autonomic and cortical correlates

Emotionally arousing pictures elicit larger late positive potentials (LPPs) than neutral pictures during passive viewing. Moreover, these cortical responses do not rely on voluntary evaluation of the hedonic content and are relatively unaffected by task demands. In this study, we examined modulation of the late positive potential as it varies with stimulus repetition. Three pictures (pleasant, neutral, unpleasant) were presented up to 60 times each. Although the amplitude of the late positive potential during picture viewing declined with stimulus repetition, affective modulation remained intact. On the other hand, autonomic responses (skin conductance and heart rate change) habituated rapidly with stimulus repetition. These findings suggest that while stimulus detection and categorization, reflected in the LPP, is mandatory, autonomic modulation reflects initial orienting responses that habituate rapidly.     

Trust at first sight: evidence from ERPs

We used event-related potentials (ERPs) to tap the temporal dynamics of first impressions based on face appearance. Participants were asked to evaluate briefly presented faces for trustworthiness and political choice. Behaviorally, participants were better at discriminating faces that were pre-rated as untrustworthy. The ERP results showed that the P100 component was enhanced for untrustworthy faces, consistently with the view that signals of potential threat are given precedence in neural processing. The enhanced ERP responses to untrustworthy faces persisted throughout the processing sequence and the amplitude of early posterior negativity (EPN), and subsequent late positive potential (LPP) was increased with respect to trustworthy faces which, in contrast, elicited an enhanced positivity around 150 ms on frontal sites. These ERP patterns were found specifically for the trustworthiness evaluation and not for the political decision task. Political decision yielded an increase in the N170 amplitude, reflecting a more demanding and taxing structural encoding. Similar ERP responses, as previously reported in the literature for facial expressions processing, were found throughout the entire time course specifically elicited by faces explicitly judged as untrustworthy. One possibility might be that evolution has provided the brain with a ‘special toolkit’ for trust evaluation that is fast and triggers ERPs related to emotional processing.     

Memory bias in anorexia nervosa: evidence from directed forgetting

The aim of this study was to examine memory bias for disorder-relevant information in anorexia nervosa by using the directed forgetting paradigm. Normal controls and patients with anorexia nervosa were given a list consisting of neutral and disorder-relevant words, which they were either asked to remember (R) or forget (F). Memory performance was measured by a free recall and a Yes/No recognition task for all items. There was a directed forgetting effect for both groups; however, the magnitude of the effect (difference between R and F words) was smaller for the patient group due to higher recall of F items. Further analyses showed that this was true only for disorder-relevant but not for neutral items. Our findings support the existence of a strong memory bias for disorder-relevant information in patients with anorexia nervosa, who had difficulty in avoiding the processing of information that they were asked to forget.     

Emotion modulates early auditory response to speech

In order to understand how emotional state influences the listener's physiological response to speech, subjects looked at emotion-evoking pictures while 32-channel EEG evoked responses (ERPs) to an unchanging auditory stimulus ("danny") were collected. The pictures were selected from the International Affective Picture System database. They were rated by participants and differed in valence (positive, negative, neutral), but not in dominance and arousal. Effects of viewing negative emotion pictures were seen as early as 20 msec (p = .006). An analysis of the global field power highlighted a time period of interest (30.4-129.0 msec) where the effects of emotion are likely to be the most robust. At the cortical level, the responses differed significantly depending on the valence ratings the subjects provided for the visual stimuli, which divided them into the high valence intensity group and the low valence intensity group. The high valence intensity group exhibited a clear divergent bivalent effect of emotion (ERPs at Cz during viewing neutral pictures subtracted from ERPs during viewing positive or negative pictures) in the time period of interest (r(Phi) = .534, p < .01). Moreover, group differences emerged in the pattern of global activation during this time period. Although both groups demonstrated a significant effect of emotion (ANOVA, p = .004 and .006, low valence intensity and high valence intensity, respectively), the high valence intensity group exhibited a much larger effect. Whereas the low valence intensity group exhibited its smaller effect predominantly in frontal areas, the larger effect in the high valence intensity group was found globally, especially in the left temporal areas, with the largest divergent bivalent effects (ANOVA, p < .00001) in high valence intensity subjects around the midline. Thus, divergent bivalent effects were observed between 30 and 130 msec, and were dependent on the subject's subjective state, whereas the effects at 20 msec were evident only for negative emotion, independent of the subject's behavioral responses. Taken together, it appears that emotion can affect auditory function early in the sensory processing stream.