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2005, Trends in Cognitive Sciences
Emotional processes not only serve to record the value of sensory events, but also to elicit adaptive responses and modify perception. Recent research using functional brain imaging in human subjects has begun to reveal neural substrates by which sensory processing and attention can be modulated by the affective significance of stimuli. The amygdala plays a crucial role in providing both direct and indirect top-down signals on sensory pathways, which can influence the representation of emotional events, especially when related to threat. These modulatory effects implement specialized mechanisms of 'emotional attention' that might supplement but also compete with other sources of top-down control on perception. This work should help to elucidate the neural processes and temporal dynamics governing the integration of cognitive and affective influences in attention and behaviour.
Biological Psychology, 2013
The rapid and efficient selection of emotionally-salient or goal-relevant stimuli in the environment is crucial for flexible and adaptive behaviors. Converging data from neuroscience and psychology have accrued during the last decade to identify brain systems involved in emotion processing, selective attention, and their interaction, which together act to extract the emotional or motivational value of sensory events and respond appropriately. An important hub in these systems is the amygdala, which may not only monitor the emotional value of stimuli, but also readily project to several other areas and send feedback to sensory pathways (including striate and extrastriate visual cortex). This system generates saliency signals that modulate perceptual, motor, as well as memory processes, and thus in turn regulate behavior appropriately. Here, we review our current views on the function and properties of these brain systems, with an emphasis on their involvement in the rapid and/or preferential processing of threat-relevant stimuli. We suggest that emotion signals may enhance processing efficiency and competitive strength of emotionally significant events through gain control mechanisms similar to those of other (e.g. endogenous) attentional systems, but mediated by distinct neural mechanisms in amygdala and interconnected prefrontal areas. Alterations in these brain mechanisms might be associated with psychopathological conditions, such as anxiety or phobia. We conclude that attention selection and awareness are determined by multiple attention gain control systems that may operate in parallel and use different sensory cues but act on a common perceptual pathway.
2005
Facial expressions of emotion elicit increased activity in the human amygdala. Such increases are particularly evident for expressions that convey potential threat to the observer, and arise even when the face is masked from awareness. We used functional magnetic resonance imaging (fMRI) to examine whether the amygdala responds differentially to threatening (fearful) versus nonthreatening (happy) facial expressions depending on whether the face is attended or actively ignored.
NeuroImage, 2007
Recent studies have cast doubts on the appealing idea that the processing of threat-related stimuli in the amygdala is unconstrained by the availability of attentional resources. However, these studies exclusively used face stimuli presented at fixation and it is unclear whether their conclusion can apply to peripheral face stimuli. Thus, we designed an experiment in which we manipulated the perceptual attentional load of the task used to divert attention from peripheral face stimuli: participants were presented simultaneously with four peripheral pictures (two faces, either both neutral or both fearful, and two houses) that were slightly tilted, and had to match two of these pictures (defined by their position on the screen) either for orientation of the tilt or for identity. The identity task was confirmed to involve greater attentional load than the orientation task by differences in accuracy, reaction times, subsequent face recognition performance, and patterns of activation in ...
Biological Psychiatry, 2009
Background: A vital component of an organism's response to acute stress is a surge in vigilance that serves to optimize the detection and assessment of threats to its homeostasis. The amygdala is thought to regulate this process, but in humans, acute stress and amygdala function have up to now only been studied in isolation. Hence, we developed an integrated design using functional magnetic resonance imaging to investigate the immediate effects of controlled stress induction on amygdala function. Methods: In 27 healthy female participants, we studied brain responses to emotional facial stimuli, embedded in an either acutely stressful or neutral context by means of adjoining movie clips. Results: A variety of physiological and psychological measures confirmed successful induction of moderate levels of acute stress. More importantly, this context manipulation shifted the amygdala toward higher sensitivity as well as lower specificity, that is, stress induction augmented amygdala responses to equally high levels for threat-related and positively valenced stimuli, thereby diminishing a threatselective response pattern. Additionally, stress amplified sensory processing in early visual regions and the face responsive area of the fusiform gyrus but not in a frontal region involved in task execution. Conclusions: A shift of amygdala function toward heightened sensitivity with lower levels of specificity suggests a state of indiscriminate hypervigilance under stress. Although this represents initial survival value in adverse situations where the risk for false negatives in the detection of potential threats should be minimized, it might similarly play a causative role in the sequelae of traumatic events.
Scientific Reports
it has been proposed that the human amygdala may not only encode the emotional value of sensory events, but more generally mediate the appraisal of their relevance for the individual's goals, including relevance for action or task-based needs. However, emotional and non-emotional/action-relevance might drive amygdala activity through distinct neural signals, and the relative timing of both kinds of responses remains undetermined. Here, we recorded intracranial event-related potentials from nine amygdalae of patients undergoing epilepsy surgery, while they performed variants of a Go/NoGo task with faces and abstract shapes, where emotion-and action-relevance were orthogonally manipulated. Our results revealed early amygdala responses to emotion facial expressions starting ~ 130 ms after stimulus-onset. Importantly, the amygdala responded to action-relevance not only with face stimuli but also with abstract shapes (squares), and these relevance effects consistently occurred in later time-windows (starting ~ 220 ms) for both faces and squares. A similar dissociation was observed in gamma activity. Furthermore, whereas emotional responses habituated over time, the actionrelevance effect increased during the course of the experiment, suggesting progressive learning based on the task needs. Our results support the hypothesis that the human amygdala mediates a broader relevance appraisal function, with the processing of emotion-relevance preceding temporally that of action-relevance. The amygdala is a crucial component of brain circuits allowing swift reaction to threatening stimuli, an ability critical for adaptive behavior and survival 1,2. Fast and efficient discrimination of potentially harmful events is a hallmark of the fear response, associated with a well-established sensitivity of the amygdala to threat information, and extensive connectivity with multiple other brain regions that act to facilitate attention, enhance memory, and promote actions 3. It has recently been questioned, however, whether the amygdala is dedicated to fear processing 1 or whether instead it may serve a broader function for the appraisal of behaviorally relevant events (see 4 for a review). There is abundant evidence that the human amygdala responds to other emotionally significant stimuli beyond threat 5 , including positive or reward information 6,7 , but also novelty 8 and non-emotional salient stimuli with personal impact or goal-related significance 9,10. This diversity of response patterns has led to recent theoretical accounts proposing that the amygdala may actually encode the "relevance" of events, which is determined by the goals,
If the amygdala is involved in shaping perceptual experience when affectively significant visual items are encountered, responses in this structure should be correlated with both visual cortex responses and behavioral reports. Here, we investigated how affective significance shapes visual perception during an attentional blink paradigm combined with aversive conditioning. Behaviorally, following aversive learning, affectively significant scenes (CS ؉ ) were better detected than neutral (CS ؊ ) ones. In terms of mean brain responses, both amygdala and visual cortical responses were stronger during CS ؉ relative to CS ؊ trials. Increased brain responses in these regions were associated with improved behavioral performance across participants and followed a mediationlike pattern. Importantly, the mediation pattern was observed in a trial-by-trial analysis, revealing that the specific pattern of trialby-trial variability in brain responses was closely related to singletrial behavioral performance. Furthermore, the influence of the amygdala on visual cortical responses was consistent with a mediation, although partial, via frontal brain regions. Our results thus suggest that affective significance potentially determines the fate of a visual item during competitive interactions by enhancing sensory processing through both direct and indirect paths. In so doing, the amygdala helps separate the significant from the mundane.
Cogent Psychology
The human amygdala consciously and nonconsciously processes facial expressions and directs spatial attention to them. Research has shown that amygdala activity habituates after repeated exposure to emotionally salient stimuli during passive viewing tasks. However, it is unclear to what extent the amygdala habituates during biologically relevant amygdala-mediated behaviors, such as the orienting of attention to environmentally salient social signals. The present study investigated amygdala habituation during a dot-probe task measuring attentional bias to backward masked fearful faces. The results suggest that across the duration of the 50 min (1,098 trial) task both attentional bias behavior and amygdala activity were sustained-rather than habituated. Thus, these initial findings indicate that when biologically relevant behavior is sustained, so too is amygdala activation.
Philosophical Transactions of the Royal Society B: Biological Sciences, 2007
Visual processing is not determined solely by retinal inputs. Attentional modulation can arise when the internal attentional state (current task) of the observer alters visual processing of the same stimuli. This can influence visual cortex, boosting neural responses to an attended stimulus. Emotional modulation can also arise, when affective properties (emotional significance) of stimuli, rather than their strictly visual properties, influence processing. This too can boost responses in visual cortex, as for fear-associated stimuli. Both attentional and emotional modulation of visual processing may reflect distant influences upon visual cortex, exerted by brain structures outside the visual system per se . Hence, these modulations may provide windows onto causal interactions between distant but interconnected brain regions. We review recent evidence, noting both similarities and differences between attentional and emotional modulation. Both can affect visual cortex, but can reflect...
The Journal of …, 2009
Models of visual emotional perception suggest a reentrant organization of the ventral visual system with the amygdala. Using focused functional magnetic resonance imaging in humans with a sampling rate of 100 ms, here we determine the relative timing of emotional discrimination in amygdala and ventral visual cortical structures during emotional perception. Results show that amygdala and inferotemporal visual cortex differentiate emotional from nonemotional scenes ϳ1 s before extrastriate occipital cortex, whereas primary occipital cortex shows consistent activity across all scenes. This pattern of discrimination is consistent with a reentrant organization of emotional perception in visual processing, in which transaction between rostral ventral visual cortex and amygdala originates the identification of emotional relevance.
Neuron, 2001
Critchley et al., 2000a), as well as the association be-Weizmann Institute for Science tween visual cortex and amygdala activation during Rehovot emotional stimulation (Dolan and Morris, 2000). Israel By contrast, lesion studies in humans demonstrated double dissociation between visual perception and the related emotional processes (Young et al., 1993; Summary Adolphs et al., 1995; Aggleton and Young, 2000). Thus, face recognition could be impaired with no impairment Emotionally loaded visual stimuli have shown inin the ability to recognize the related emotional exprescreased activation in visual and cortex limbic areas. sion as shown in prosopagnostic (Sergent and Villemure, However, differences in visual features of such images 1989; de Gelder et al., 2000; Bauer, 1984; Tranel and could confound these findings. In order to manipulate Damasio, 1988) or hemifield blind-sight patient (de valence of stimuli while keeping visual features largely Gelder et al., 1999). In equivalent vein, emotional deficits unchanged, we took advantage of an "expressional did not entail visual deficits in patients with amygdala transfiguration" (ET) effect of faces. In addition, we lesions (Adolphs et al., 1994, 1995; Young et al., 1995, used repetition effects, which enabled us to test more 1996; Calder et al., 1996; Bechara et al., 1995). Finally, incisively the impact of the ET effect. Using the ET single cell recordings in primates showed that magnimanipulation, we have shown that the activation in tude of neuronal activation in the inferior temporal cortex lateral occipital complex (LOC) was unaffected by vawas not affected by the associated valence of the stimlence attributes, but produced significant modulation uli, generated by reward (Rolls et al., 1977). Similarly, of fMR adaptation. Contrary to LOC, amygdala activafunctional brain imaging in humans showed that negation was increased by ET manipulation unrelated to tively conditioned faces did not elicit different activation the adaptation. A correlation between amygdala and in the visual cortex compared to unconditioned faces LOC adaptation points to a possible modulatory role of (Buchel et al., 1998). Thus, emotional context alone does the amygdala upon visual cortex short-term plasticity. not seem to affect visual cortex activation. One possible explanation for the above discrepancy D. (2000a). Explicit and implicit neural mechanisms for processing of social information from facial expressions: a functional magnetic resonance imaging study. Hum. Brain Mapp. 9, 93-105. Adolphs, R., Tranel, D., Damasio, H., and Damasio, A.R. (1994). Impaired recognition of emotion in facial expressions following bilat-Critchley, H.D., Elliott, R., Mathias, C., and Dolan, R. (2000b). Neural eral damage to the human amygdala. Nature 372, 669-672. activity relating to generation and representation of galvanic skin conductance responses: a functional magnetic resonance imaging Adolphs, R., Tranel, D., Damasio, H., and Damasio, A.R. (1995). Fear study. J. Neurosci. 20, 3033-3040. and the human amygdala. J. Neurosci. 15, 5879-5891. Davis, M. (1992). The role of the amygdala in fear and anxiety. Annu. Aggleton, J.P., and Young, A.W. (2000). The enigma of the amygdala: Rev. Neurosci. 15, 353-375. on its contribution to human emotion.
NeuroImage, 2008
2006
The amygdala has been consistently isolated as a key neural substrate for processing facial displays of affect. Recent evidence from human lesion and functional neuroimaging studies have begun to challenge the notion that the amygdala is reserved for signals of threat (fear/anger). We performed a 4 T fMRI study in which 20 subjects viewed a contemporary set of photographs displaying 6 different facial expressions (fearful, disgusted, angry, sad, neutral, happy) while performing a task with minimal cognitive demand. Across subjects, the left amygdala was activated by each face condition separately, and its response was not selective for any particular emotion category. These results challenge the notion that the amygdala has a specialized role in processing certain emotions and suggest that the amygdala may have a more general-purpose function in processing salient information from faces. D
Neuroscience & Biobehavioral Reviews, 2012
While the amygdalar role in fear conditioning is well established, it also appears to be involved in a wide spectrum of other functions concerning emotional information. For example, the amygdala is thought to be involved in guiding spatial attention to emotionally relevant information such as the eye region in faces, and it gets activated differentially during different tasks. Here, we propose that the guidance of feature-based attention is the basis for the involvement of the amygdala in these seemingly disparate functions. Feature-based attention usually precedes spatial attention, and performing different tasks usually requires attending to different features. Although to date, no experiments have specifically tested the amygdalar role in feature-based attention, studies showing that the amygdala responds to simple elements, and findings of amygdalar involvement in non-spatial forms of attention hint at such a role. Our hypothesis that the amygdala guides feature-based attention builds on earlier proposals that the amygdala guides spatial attention and assesses biological relevance, but it is more specific and accounts for the failure to find amygdalar activation when spatial cues guide attention. Our hypothesis results in the testable prediction that the amygdala is involved when searching for stimuli based on their feature information, but not when searching for stimuli based on spatial cues.
Biological Psychology, 2010
Neuropsychologia, 2011
The importance of cues signaling reward, threat or danger would suggest that they receive processing privileges in the neural systems underlying perception and attention. Previous research has documented enhanced processing of motivationally salient cues, and has pointed to the amygdala as a candidate neutral structure underlying the enhancements. In the current study, we examined whether the amygdala was necessary for this emotional modulation of attention to occur. Patients with unilateral amygdala lesions and matched controls completed an emotional attentional blink task in which emotional distractors impair the perception of subsequent targets. Emotional images proved more distracting across all participant groups, including those with right or left amygdala lesions. These data argue against a central role for the amygdala in mediating all types of attentional capture by emotional stimuli. * Anderson and Phelps (2001) refer to this 'breaking through' as capturing attention. To avoid confusion, we will refer to the phenomenon described in the present study, attentional capture that prevents detection of subsequent stimuli, as attentional
2020
The human amygdala consciously and nonconsciously processes facial expressions and directs spatial attention to them. Research has shown that amygdala activity habituates after repeated exposure to emotionally salient stimuli during passive viewing tasks. However, it is unclear to what extent the amygdala habituates during biologically relevant amygdala-mediated behaviors, such as the orienting of attention to environmentally salient social signals. The present study investigated amygdala habituation during a dot-probe task measuring attentional bias to backward masked fearful faces. The results suggest that across the duration of the 50 min (1,098 trial) task both attentional bias behavior and amygdala activity were sustained—rather than habituated. Thus, these initial findings indicate that when biologically relevant behavior is sustained, so too is amygdala activation. Subjects: Neuroscience; Psychological Science; Attention; Emotion; Cognition & Emotion; Cognitive Neuroscience; ...
It has been shown that as cognitive demands of a non-emotional task increase, amygdala response to task-irrelevant emotional stimuli is reduced. However, it remains unclear whether effects are due to altered task demands, or altered perceptual input associated with task demands. Here, we present fMRI data from 20 adult males during a novel cognitive conflict task in which the requirement to scan emotional information was necessary for task performance and held constant across levels of cognitive conflict. Response to fearful facial expressions was attenuated under high (vs low) conflict conditions, as indexed by both slower reaction times and reduced right amygdala response. Psychophysiological interaction analysis showed that increased amygdala response to fear in the low conflict condition was accompanied by increased functional coupling with middle frontal gyrus, a prefrontal region previously associated with emotion regulation during cognitive task performance. These data suggest that amygdala response to emotion is modulated as a function of task demands, even when perceptual inputs are closely matched across load conditions. PPI data also show that, in particular emotional contexts , increased functional coupling of amygdala with prefrontal cortex can paradoxically occur when executive demands are lower.
Department of Psychology, New York University, 2006
This review explores insights into the relations between emotion and cognition that have resulted from studies of the human amygdala. Five topics are explored: emotional learning, emotion and memory,emotion’s influence on attention and perception, processing emotion in social stimuli, and changing emotional responses.
Frontiers in human neuroscience, 2014
The amygdala has been implicated in the processing of emotion and animacy information and to be responsive to novelty. However, the way in which these functions interact is poorly understood. Subjects (N = 30) viewed threatening or neutral images that could be either animate (facial expressions) or inanimate (objects) in the context of a dot probe task. The amygdala showed responses to both emotional and animacy information, but no emotion by stimulus-type interaction; i.e., emotional face and object stimuli, when matched for arousal and valence, generate comparable amygdala activity relative to neutral face and object stimuli. Additionally, a habituation effect was not seen in amygdala; however, increased amygdala activity was observed for incongruent relative to congruent negative trials in second vs. first exposures. Furthermore, medial fusiform gyrus showed increased response to inanimate stimuli, while superior temporal sulcus showed increased response to animate stimuli. Great...
2007
The current study examined the hypothesis that amygdala activation serves as a neural precondition for negative affective experience. Participants' affective experience was measured by asking them to report on their momentary experiences several times a day over the course of a month using an electronic experience-sampling procedure. One year later, participants viewed backwardly masked depictions of fear while functional magnetic resonance imaging was used to measure their amygdala and fusiform gyrus activation. Negative affect, as measured during the experience-sampling procedure 1-year prior, was positively correlated with amygdala activation in response to these brief presentations of fear depictions. Furthermore, descriptive analyses indicated that fusiform gyrus activation and negative affective experience in the scanner were associated for participants reporting increased nervousness during the imaging procedure. The results are consistent with the interpretation that the amygdala contributes to negative affective experience by increasing perceptual sensitivity for negative stimuli. Negative affect and perceptual sensitivity Converging evidence from research on both clinical and normal samples suggests that people who routinely experience negative affect show a perceptual sensitivity to negative
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