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Several recent studies using functional magnetic resonance imaging (fMRI) during recognition memory tests have suggested that the ability to neuromodulate as a function of cognitive demand may be impaired in older adults due to age-related cell loss and neural volume reduction in memory specific regions. In the current study, older adults (ages 59-77) were tested with fMRI during a delayed-recognition task in which memory load for faces was varied across trials. Activity was greater in amplitude for three- versus one-face stimuli within the superior, middle, and inferior frontal gyri, intraparietal sulcus, and fusiform gyrus. It was concluded that the ability to modulate activity with increasing load is preserved in older adults despite reductions in neural volume.
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To monitor the environment for social threat humans must build affective evaluations of others. These evaluations are malleable and to a high degree shaped by responses engendered by specific social encounters. The precise neuronal mechanism by which these evaluations are constructed is poorly understood. We tested a hypothesis that conjoint activity in amygdala and fusiform gyrus would correlate with acquisition of social stimulus value. We tested this using a reinforcement learning algorithm, Q-learning, that assigned values to faces as a function of a history of pairing, or not pairing, with aversive shocks. Behaviourally, we observed a correlation between conditioning induced changes in skin conductance response (SCR) and subjective ratings for likeability of faces. Activity in both amygdala and fusiform gyrus (FG) correlated with the output of the reinforcement learning algorithm parameterized by these ratings. In amygdala, this effect was greater for averted than direct gaze faces. Furthermore, learning-related activity change in these regions correlated with SCR and subjective ratings. We conclude that amygdala and fusiform encode affective value in a manner that closely approximates a standard computational solution to learning.
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Positive affect elicited in a mother toward her newborn infant may be one of the most powerful and evolutionarily preserved forms of positive affect in the emotional landscape of human behavior. This study examined the neurobiology of this form of positive emotion and in so doing, sought to overcome the difficulty of eliciting robust positive affect in response to visual stimuli in the physiological laboratory. Six primiparous human mothers with no indications of postpartum depression brought their infants into the laboratory for a photo shoot. Approximately 6 weeks later, they viewed photographs of their infant, another infant, and adult faces during acquisition of functional magnetic resonance images (fMRI). Mothers exhibited bilateral activation of the orbitofrontal cortex (OFC) while viewing pictures of their own versus unfamiliar infants. While in the scanner, mothers rated their mood more positively for pictures of their own infants than for unfamiliar infants, adults, or at baseline. The orbitofrontal activation correlated positively with pleasant mood ratings. In contrast, areas of visual cortex that also discriminated between own and unfamiliar infants were unrelated to mood ratings. These data implicate the orbitofrontal cortex in a mother's affective responses to her infant, a form of positive emotion that has received scant attention in prior human neurobiological studies. Furthermore, individual variations in orbitofrontal activation to infant stimuli may reflect an important dimension of maternal attachment.
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Social relations between humans critically depend on our affective experiences of others. Oxytocin enhances prosocial behavior, but its effect on humans' affective experience of others is not known. We tested whether oxytocin influences affective ratings, and underlying brain activity, of faces that have been aversively conditioned. Using a standard conditioning procedure, we induced differential negative affective ratings in faces exposed to an aversive conditioning compared with nonconditioning manipulation. This differential negative evaluative effect was abolished by treatment with oxytocin, an effect associated with an attenuation of activity in anterior medial temporal and anterior cingulate cortices. In amygdala and fusiform gyrus, this modulation was stronger for faces with direct gaze, relative to averted gaze, consistent with a relative specificity for socially relevant cues. The data suggest that oxytocin modulates the expression of evaluative conditioning for socially relevant faces via influences on amygdala and fusiform gyrus, an effect that may explain its prosocial effects.
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Individuals with fragile X syndrome (FXS) commonly display characteristics of social anxiety, including gaze aversion, increased time to initiate social interaction, and difficulty forming meaningful peer relationships. While neural correlates of face processing, an important component of social interaction, are altered in FXS, studies have not examined whether social anxiety in this population is related to higher cognitive processes, such as memory. This study aimed to determine whether the neural circuitry involved in face encoding was disrupted in individuals with FXS, and whether brain activity during face encoding was related to levels of social anxiety. A group of 11 individuals with FXS (5 M) and 11 age- and gender-matched control participants underwent fMRI scanning while performing a face encoding task with online eye-tracking. Results indicate that compared to the control group, individuals with FXS exhibited decreased activation of prefrontal regions associated with complex social cognition, including the medial and superior frontal cortex, during successful face encoding. Further, the FXS and control groups showed significantly different relationships between measures of social anxiety (including gaze-fixation) and brain activity during face encoding. These data indicate that social anxiety in FXS may be related to the inability to successfully recruit higher level social cognition regions during the initial phases of memory formation.
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Working memory (WM) comprises operations whose coordinated action contributes to our ability to maintain focus on goal-relevant information in the presence of distraction. The present study investigated the nature of distraction upon the neural correlates of WM maintenance operations by presenting task-irrelevant distracters during the interval between the memoranda and probes of a delayed-response WM task. The study used a region of interest (ROIs) approach to investigate the role of anterior (e.g., lateral and medial prefrontal cortex--PFC) and posterior (e.g., parietal and fusiform cortices) brain regions that have been previously associated with WM operations. Behavioral results showed that distracters that were confusable with the memorandum impaired WM performance, compared to either the presence of non-confusable distracters or to the absence of distracters. These different levels of distraction led to differences in the regional patterns of delay interval activity measured with event-related functional magnetic resonance imaging (fMRI). In the anterior ROIs, dorsolateral PFC activation was associated with WM encoding and maintenance, and in maintaining a preparatory state, and ventrolateral PFC activation was associated with the inhibition of distraction. In the posterior ROIs, activation of the posterior parietal and fusiform cortices was associated with WM and perceptual processing, respectively. These findings provide novel evidence concerning the neural systems mediating the cognitive and behavioral responses during distraction, and places frontal cortex at the top of the hierarchy of the neural systems responsible for cognitive control.
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Selective attention has been shown to bias sensory processing in favor of relevant stimuli and against irrelevant or distracting stimuli in perceptual tasks. Increasing evidence suggests that selective attention plays an important role during working memory maintenance, possibly by biasing sensory processing in favor of to-be-remembered items. In the current study, we investigated whether selective attention may also support working memory by biasing processing against irrelevant and potentially distracting information. Event-related potentials (ERPs) were recorded while subjects (n = 22) performed a delayed-recognition task for faces and shoes. The delay period was filled with face or shoe distractors. Behavioral performance was impaired when distractors were congruent with the working memory domain (e.g., face distractor during working memory for faces) relative to when distractors were incongruent with the working memory domain (e.g., face distractor during shoe working memory). If attentional biasing against distractor processing is indeed functionally relevant in supporting working memory maintenance, perceptual processing of distractors is predicted to be attenuated when distractors are more behaviorally intrusive relative to when they are nonintrusive. As such, we predicted that perceptual processing of distracting faces, as measured by the face-sensitive N170 ERP component, would be reduced in the context of congruent (face) working memory relative to incongruent (shoe) working memory. The N170 elicited by distracting faces demonstrated reduced amplitude during congruent versus incongruent working memory. These results suggest that perceptual processing of distracting faces may be attenuated due to attentional biasing against sensory processing of distractors that are most behaviorally intrusive during working memory maintenance.
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The development of functional neuroimaging of emotion holds the promise to enhance our understanding of the biological bases of affect and improve our knowledge of psychiatric diseases. However, up to this point, researchers have been unable to objectively, continuously and unobtrusively measure the intensity and dynamics of affect concurrently with functional magnetic resonance imaging (fMRI). This has hindered the development and generalizability of our field. Facial electromyography (EMG) is an objective, reliable, valid, sensitive, and unobtrusive measure of emotion. Here, we report the successful development of a method for simultaneously acquiring fMRI and facial EMG. The ability to simultaneously acquire brain activity and facial physiology will allow affective neuroscientists to address theoretical, psychiatric, and individual difference questions in a more rigorous and generalizable way.
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We investigated the top-down influence of working memory (WM) maintenance on feedforward perceptual processing within occipito-temporal face processing structures. During event-related potential (ERP) recordings, subjects performed a delayed-recognition task requiring WM maintenance of faces or houses. The face-sensitive N170 component elicited by delay-spanning task-irrelevant grayscale noise probes was examined. If early feedforward perceptual activity is biased by maintenance requirements, the N170 ERP component elicited by probes should have a greater N170 amplitude response during face relative to house WM trials. Consistent with this prediction, N170 elicited by probes presented at the beginning, middle, and end of the delay interval was greater in amplitude during face relative to house WM. Thus, these results suggest that WM maintenance demands may modulate early feedforward perceptual processing for the entirety of the delay duration. We argue based on these results that temporally early biasing of domain-specific perceptual processing may be a critical mechanism by which WM maintenance is achieved.
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Facial expressions of pain are an important part of the pain response, signaling distress to others and eliciting social support. To evaluate how voluntary modulation of this response contributes to the pain experience, 29 subjects were exposed to thermal stimulation while making standardized pain, control, or relaxed faces. Dependent measures were self-reported negative effect (valence and arousal) as well as the intensity of nociceptive stimulation required to reach a given subjective level of pain. No direct social feedback was given by the experimenter. Although the amount of nociceptive stimulation did not differ across face conditions, subjects reported more negative effects in response to painful stimulation while holding the pain face. Subsequent analyses suggested the effects were not due to preexisting differences in the difficulty or unpleasantness of making the pain face. These results suggest that voluntary pain expressions have no positively reinforcing (pain attenuating) qualities, at least in the absence of external contingencies such as social reinforcement, and that such expressions may indeed be associated with higher levels of negative affect in response to similar nociceptive input. PERSPECTIVE: This study demonstrates that making a standardized pain face increases negative affect in response to nociceptive stimulation, even in the absence of social feedback. This suggests that exaggerated facial displays of pain, although often socially reinforced, may also have unintended aversive consequences.
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Working memory (WM) representations serve as templates that guide behavior, but the neural basis of these templates remains elusive. We tested the hypothesis that WM templates are maintained by biasing activity in sensoriperceptual neurons that code for features of items being held in memory. Neural activity was recorded using event-related potentials (ERPs) as participants viewed a series of faces and responded when a face matched a target face held in WM. Our prediction was that if activity in neurons coding for the features of the target is preferentially weighted during maintenance of the target, then ERP activity evoked by a nontarget probe face should be commensurate with the visual similarity between target and probe. Visual similarity was operationalized as the degree of overlap in visual features between target and probe. A face-sensitive ERP response was modulated by target-probe similarity. Amplitude was largest for probes that were similar to the target, and decreased monotonically as a function of decreasing target-probe similarity. These results indicate that neural activity is weighted in favor of visual features that comprise an actively held memory representation. As such, our findings support the notion that WM templates rely on neural populations involved in forming percepts of memory items.
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