Attention and emotion

From Scholarpedia

Author: Dr. Luiz Pessoa, Indiana University, Bloomington, IN

Co-authors: Leticia Oliveira and Mirtes G. Pereira, Department of Physiology and Pharmacology, Federal Fluminense University, Rio de Janeiro, Brazil

The processing of emotion-laden visual stimuli is often proposed to take place in an automatic fashion that takes place independently of top-down factors such as attention and awareness. Studies during the current decade suggest instead that affective processing is, in many circumstances, under the control of attention.

Prioritization

A host of different experimental paradigms have documented the many ways in which the processing of emotion-laden stimuli is prioritized. These include detection, search, interference, masking, and the attentional blink, to name just a few of the main ones. For instance, during the attentional blink paradigm, subjects are asked to report both a first (T1) and a second (T2) visual target within a stream of distractor items. Detecting a second target is believed to be hampered by the initial T1 processing (due to limited processing resources). Interestingly, an emotional T2 item is better detected than a corresponding neutral one, suggesting that the affective dimension of the item counteracts the “blink” (Anderson and Phelps, 2001; Anderson, 2005). The mechanisms underlying affective prioritization continue to be the target of much research, but are generally believed to be related to increased sensory processing to affective stimuli. Indeed, relative to neutral stimuli, emotional stimuli evoke increased fMRI responses across all of ventral occipito-temporal cortex, including “early”, “intermediate”, and “late” visual areas. For instance, Bradley and colleagues (2003) reported more extensive visual cortex activity when participants viewed emotional, compared to neutral, pictures. Furthermore, Padmala and Pessoa (2008) showed a close link between improvements in behavioral performance and trial-by-trial responses in early visual cortex (including primary visual cortex) during the processing of affectively significant visual items. Increased cortical responses in visual cortex to affective stimuli may be due to modulatory signals from the amygdala, consistent with the existence of efferent projections from this structure that reach many levels of the visual cortex (Amaral et al., 1992). Indeed, patients with amygdala lesions failed to exhibit differential responses in visual cortex when viewing emotional faces (Vuilleumier et al., 2004).

Attention is not required for emotional perception

Figure 1: Attention is not required for the processing of emotional stimuli. (A) Paradigm employed to manipulate the spatial focus of attention during the presentation of emotional faces. (B) Activation in the left amygdala to fearful vs. neutral faces irrespective of the focus of attention. Adapted from Vuilleumier et al. (2001) with permission.

Affective stimuli effectively divert processing resources and interfere with performance even when they are task irrelevant (Pessoa and Ungerleider, 2004; Vuilleumier, 2005). For instance, RTs when subjects performed auditory tasks (e.g., word discrimination) were slower when they viewed distractor pictures that were unpleasant relative to neutral ones (Bradley et al., 1996; Buodo et al., 2002). Strikingly, such interference has been observed even when the primary task is a very basic one, such as the detection of a simple visual stimulus (Pereira et al., 2006). The interference effects are not only evident in terms of behavioral performance, but are also manifested physiologically. For example, specific event-related potential (ERP) components due to picture viewing were modulated by emotional content even when the main task involved simply detecting a checkerboard stimulus that was interspersed with picture presentation (Schupp et al., 2003). Together, these studies are often interpreted as supporting the notion that the processing of emotional stimuli is obligatory and that increased processing resources are allocated toward their processing although they are irrelevant to the task at hand. A stronger argument can be advanced that emotional processing is obligatory based on studies in which the spatial focus of attention is explicitly manipulated – note that in the experiments of the previous paragraph, although task irrelevant, emotional stimuli were fully attended. In a well-known study (Vuilleumier et al., 2001), the attentional focus was manipulated by having subjects maintain central fixation while they were asked to compare either two faces or two houses presented eccentrically. On each trial, subjects either compared the faces to each other or the houses to each other (see Fig. 1). Thus, the focus of attention was varied by having subjects attend to the left and the right of fixation (while ignoring top/bottom stimuli) or above and below fixation (while ignoring left/right stimuli). In each case, they indicated whether the attended stimuli were the same or not. When conditions involving fearful faces were contrasted to those involving neutral ones, differential responses in the amygdala – which is often considered as a “signature” of emotional processing – and visual cortex were not modulated by the focus of attention, consistent with the view that the processing of emotional items does not require attention. Similar findings have been reported by manipulating object-based attention while maintaining the spatial locus of attention constant (Anderson et al., 2003).

Attention is required for emotional perception

Figure 2: Attention is required for the processing of emotional stimuli. (A) Paradigm employed to manipulate the spatial focus of attention. During the attended condition, participants indicated whether faces were male or female. During the unattended condition, subjects indicated whether the peripheral bars were like oriented or not. Stimuli are not drawn to scale. The dashed ellipses indicate the locus of attention, but were not present in the actual experiment. (B) The left map illustrates the responses to the contrast attended vs. unattended when fearful faces were shown, illustrating a robust modulation of amygdala responses by attention (see circles). The panel on the right illustrates evoked responses in the left amygdala as a function of facial expression and attention, showing that differential responses were only observed during the attended condition. ATT: attended; UNATT: unattended. Results from Pessoa et al. (2002).

The argument so far can be summarized as follows. Emotional stimuli comprise a privileged stimulus category that is not only prioritized but their processing also takes place in an obligatory fashion that is independent of attention. However, it is also known that, in general, visual processing capacity is limited. Because of this finite capacity, competition among visual items is proposed to “select” the most important information at any given time (Grossberg, 1980; Desimone and Duncan, 1995). When resources are not fully consumed, it has been suggested that spare processing capacity is utilized for the processing of unattended items (Lavie, 1995). This line of reasoning, which has been applied to regular, non-emotional stimuli, suggests that the automaticity of affective processing can be tested by attentional manipulations that more fully consume available processing resources. Thus, in this context, a critical variable in understanding the extent of unattended processing is the attentional load of a task – namely, the extent to which it uses up resources. Several fMRI studies have attempted to follow the strategy outlined above. For example, the responses evoked by centrally presented emotional faces were evaluated when a very demanding peripheral task was performed. Under these conditions, differential responses to fearful vs. neutral faces were eliminated in both the amygdala and visual cortex (Pessoa et al., 2002). Consistent with the notion that task load was important in determining the extent of processing of the face stimuli, when the difficulty of the peripheral task was parametrically manipulated, a valence effect (i.e,, fearful > neutral) was observed during low task demand conditions, but not during medium or high demand conditions (Pessoa et al, 2005). The dependence of emotional perception on attention was also observed in studies that employed centrally presented, overlapping competing stimuli (i.e., paradigms that manipulate object-based attention), (Mitchell et al., 2007), including emotional stimuli of higher affective significance that were paired with shock (Lim et al., 2008) – or by using highly aversive, mutilation pictures (Erthal et al., 2005). Finally, attentional modulation of emotional perception has also been observed for peripherally presented faces (Silvert et al., 2007), a class of stimuli that may be especially effective at engaging the amygdala given that this structure may be sensitive to low spatial frequency information (Vuilleumier et al., 2003). ERP studies, which unlike fMRI studies offer temporal information on the order of milliseconds, have also investigated how emotional perception depends on attentional factors. In one study (Schupp et al., 2007), the processing of emotional items was strongly attenuated (as measured by an ERP component labeled the “EPN”) when participants performed demanding attention tasks. On the contrary, passively viewing the same emotional images generated enlarged evoked responses relative to those evoked by neutral stimuli.

Attention is not required for emotional perception (again)

The results suggesting that emotional perception is automatic or that it depends on attention can be reconciled by making use of the concept of attentional load (Lavie, 1995). When load is low, “spill over” capacity is available to the processing of task-irrelevant emotional stimuli. As load is increased, however, fewer resources will be available and, in the limit, emotional perception will be eliminated. Whereas this framework can be used to explain a broad set of results, some findings appear to resist this explanation. In one study (Muller et al., 2008), emotionally arousing background pictures appeared to divert processing resources from a demanding visual target detection task (as reflected by reductions in steady-state visual evoked potentials relative to neutral pictures). In another EEG study, increased evoked responses to pleasant and unpleasant pictures (relative to neutral) were observed independently of the demand level of a concurrent auditory task (Schupp et al., 2008).

Summary

Taken together, results from behavioral and neuroimaging methods suggest that while emotional processing is prioritized, in many contexts it depends on processing resources. These findings come from diverse paradigms, including those employing peripheral emotional stimuli and those in which affective and neutral stimuli are spatially separated. In general, the discrepancy between studies suggesting that emotional perception is automatic and those illustrating the dependence on attention is accounted by the concept of attentional load. Thus, to reveal that emotional perception is not immune to the effects of attention, processing resources need to be largely consumed – otherwise, performance will appear to be relatively automatic. Yet, as outlined in the previous section, this account may not explain all cases, and there may be circumstances in which more true automaticity is observed. At present, the reasons for this discrepancy are unclear, suggesting that it would be profitable for future studies to tackle this issue more directly. One possibility is that individual differences are important predictors of amygdala sensitivity to emotional stimuli and help explain the impact of emotional stimuli (Bishop, 2007), although attention appears to be important even for high-anxious individuals (Fox et al., 2005; Bishop et al., 2007).

References

• Amaral DG, Price JL, Pitkanen A, Carmichael ST (1992) Anatomica organization of the primate amygdaloid complex. In: Anggleton JP, editor. The amygdala: neurobiological aspects of emotion, memory and mental dysfunction. New York: Wiley-Liss; p. 1-66.

• Anderson AK (2005) Affective influences on the attentional dynamics supporting awareness. J Exp Psychol Gen 134(2):258-81.

• Anderson AK, Christoff K, Panitz D, De Rosa E, Gabrieli JD (2003) Neural correlates of the automatic processing of threat facial signals. J Neurosci 23(13):5627-33.

• Anderson AK, Phelps EA (2001) Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature 17; 411(6835):305-9.

• Bishop SJ (2007) Neurocognitive mechanisms of anxiety: an integrative account. Trends Cogn Sci 11:307-316.

• Bishop SJ, Jenkins R, Lawrence AD (2007) Neural processing of fearful faces: effects of anxiety are gated by perceptual capacity limitations. Cereb Cortex 17:1595-1603.

• Bradley MM, Cuthbert BN, Lang PJ (1996) Picture media and emotion: effects of a sustained affective context. Psychophysiology 33(6):662-70.

• Bradley MM, Sabatinelli D, Lang PJ, Fitzsimmons JR, King W, Desai P (2003) Activation of the visual cortex in motivated attention. Behav Neurosci 117(2):369-80.

• Buodo G, Sarlo M, Palomba D (2002) Attentional resources measured by reaction times highlight differences within pleasant and unpleasant, high arousing stimuli. Motivation and Emotion 26: 123–138.

• Desimone R, Duncan J (1995) Neural mechanisms of selective attention. Annual Review of Neuroscience 18:193-222.

• Erthal FS, de Oliveira L, Mocaiber I, Pereira MG, Machado-Pinheiro W, Volchan E, Pessoa L (2005) Load-dependent modulation of affective picture processing. Cogn Affect Behav Neurosci. 5(4):388-95.

• Fox E, Russo R, Georgiou GA (2005) Anxiety modulates the degree of attentive resources required to process emotional faces. Cogn Affect Behav Neurosci 5(4):396-404.

• Grossberg S (1980) How does a brain build a cognitive code? Psychol Rev 87:1–51.

• Lavie, N (1995) Perceptual load as a necessary condition forselective attention. J Exp Psychol Human 21: 451–468.

• Lim SL, Pessoa L. (2008) Affective learning increases sensitivity to graded emotional faces. Emotion 8(1):96-103.

• Mitchell DG, Nakic M, Fridberg D, Kamel N, Pine DS, Blair RJ (2007) The impact of processing load on emotion. Neuroimage 34(3):1299-309.

• Müller MM, Andersen SK, Keil A (2008) Time course of competition for visual processing resources between emotional pictures and foreground task. Cereb Cortex 18(8):1892-9.

• Padmala S, Pessoa L (2008) Affective learning enhances visual detection and responses in primary visual cortex. J Neurosci 28(24):6202-10.

• Pereira MG, Volchan E, de Souza GG, Oliveira L, Campagnoli RR, Pinheiro WM, Pessoa L (2006) Sustained and transient modulation of performance induced by emotional picture viewing. Emotion 6(4):622-34.

• Pessoa L, Ungerleider LG (2004) Neuroimaging studies of attention and the processing of emotion-laden stimuli. Prog Brain Res 144:171-182.

• Pessoa L, McKenna M, Gutierrez E, Ungerleider LG (2002) Neural processing of emotional faces requires attention. Proc Natl Acad Sci 99(17):11458-63.

• Pessoa L, Padmala S, Morland T (2005) Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation. Neuroimage 28(1):249-55.

• Schupp HT, Junghöfer M, Weike AI, Hamm AO (2003) Attention and emotion: an ERP analysis of facilitated emotional stimulus processing. Neuroreport 14(8):1107-10.

• Schupp HT, Stockburger J, Bublatzky F, Junghöfer M, Weike AI, Hamm AO (2007) Explicit attention interferes with selective emotion processing in human extrastriate cortex. BMC Neurosci 8:16.

• Schupp HT, Stockburger J, Bublatzky F, Junghöfer M, Weike AI, Hamm AO (2008) The selective processing of emotional visual stimuli while detecting auditory targets: an ERP analysis. Brain Res. 1230:168-76.
• Silvert L, Lepsien J, Fragopanagos N, Goolsby B, Kiss M, Taylor JG, Raymond JE, Shapiro KL, Eimer M, Nobre AC (2007) Influence of attentional demands on the processing of emotional facial expressions in the amygdale Neuroimage 38(2):357-66.

• Vuilleumier P, Armony JL, Driver J, Dolan RJ (2001) Effects of attention and emotion on face processing in the human brain: an event-related fMRI study. Neuron 30(3):829-41.

• Vuilleumier P, Armony JL, Driver J, Dolan RJ (2003) Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nat Neurosci 6(6):624-31.

• Vuilleumier P, Richardson MP, Armony JL, Driver J, Dolan RJ (2004) Distant influences of amygdala lesion on visual cortical activation during emotional face processing. Nat Neurosci 7(11):1271-8.

• Vuilleumier P (2005) How brains beware: neural mechanisms of emotional attention. Trends Cogn Sci. 9(12):585-94.

External links

• Luiz Pessoa's website