Talk:Attention and emotion
We are indebted to the reviewers for their very thoughtful and constructive comments. Where possible, we have addressed the suggestions, which are marked below in bold font and in the same manner in the main text to facilitate the review process. In several instances, it was not possible to incorporate suggestions given that it would have altered the flow of the piece considerably and would have extended the scope considerably beyond the original goal of providing a succinct, yet up to date, review of the findings on attention and emotion.
Reviewer A
This review article on attention and emotion is excellent. Given the sheer breadth of the topic, my major suggestions involve a broadening of the scope of the review and (if space permits) the inclusion of more of the literature.
The article adopts a cognitive neuroscience approach and focuses primarily on the issue of whether attention is required for the processing of emotional stimuli, but it might be useful to convey how this topic fits within the context of the broader literature. For example, influential models of anxiety disorders suggest a prominent role for emotion-driven attentional biases (e.g., work by Mogg & Bradley; Williams, Watts, MacLeod, & Mathews; etc.), which have sometimes proposed that emotional processing occurs “pre-attentively” and is followed by characteristic patterns of attentional deployment that depend on an individual’s anxiety level. A brief mention of such work would help underscore why the work described in the current review should be of interest to a wide array of psychological scientists [See 1.1 in text].
There are also a number of additional questions about attention and emotion that are addressed in the literature, discussion of which might help enrich the current review. These include: 1) given evidence that emotional stimuli “capture” attention, does this occur because people tend to orient to emotional stimuli or because people have difficulty disengaging from emotional stimuli once they have attended to them (e.g., Fox et al., 2001; Fox et al., 2002)? Note that evidence for the former would be more in line with the notion that emotional stimuli can be processed without attention, and evidence of the latter would be more in line with the notion that attention is required for processing of emotional stimuli [See 1.2 in text]. 2) What is the influence of emotional state on attention? The current review emphasizes the prioritization of emotional stimuli and the degree to which attention is required for processing emotional stimuli, but the literature also contains research exploring the influence of emotional state on attention (e.g., work by Fredrickson and colleagues; Jefferies, Smilek, Eich, & Enns; Compton; etc). Readers might find it useful to see a brief mention of such work [See 1.3 in text]. 3) In addition to emotion’s impact on attention, readers might be interested in recent work suggesting a reciprocal relationship, with selective attention and selective ignoring helping to drive subsequent emotional responses to stimuli (e.g., work by Raymond and colleagues). 4) To what degree do are attention-emotion effects driven by “valence” (i.e., positive vs. negative) or “arousal”? 5) It might be useful to briefly discuss the types of emotional stimuli typically used in such research, including emotional faces, IAPS pictures, emotional words, conditioned stimuli, etc.
Of course, there are trade-offs in choosing to cover these additional considerations: although the result would be a more comprehensive review, the article’s cohesiveness might inevitably suffer. As it stands, the authors have primarily focused on a couple of the most central questions regarding attention-emotion interactions. Whereas consideration #1 suggested above might easily be integrated into the current article, it might be more difficult to incorporate consideration #2 or #3 in a similarly cohesive fashion.
Additional references that would be relevant to the current version of the article include Harris & Pashler, 2004, who found behavioral evidence that emotional stimuli are prioritized only under low perceptual load, as well as work showing that emotional stimuli not only defeat the attentional blink but also elicit spontaneous attentional blinks for other stimuli (e.g., by Most and colleagues; Arnell and colleagues; etc). In the last sentence of the “Priortization” paragraph, the previously cited article by Anderson & Phelps (2001) is relevant, as emotional stimuli failed to defeat the attentional blink among patients with amygdala damage [See 1.4 in text].
In sum, this valuable article reviews what are among the most central issues in the study of attention-emotion interactions. My only recommendation for improvement would be to broaden its scope.
Reviewer B
This article is a thorough, clear and concise review of current research on emotion and attention. The authors draw on a limited resource model to account for discrepancies between a body of evidence suggesting that prioritized perceptual processing of emotionally salient stimuli is automatic, and can occur outside of awareness, and a body of evidence indicating that attention is required for processing of emotional salience. My comments focus on interpretation of the role of the amygdala in stimulus processing, the role of emotional valence in attention/emotion interactions, and the role of individual differences in selective attention.
The Role of the Amygdala
First, as this article points out, the studies reviewed here predominantly viewed amygdala activation as a signature of emotional processing; however, it is important to acknowledge that this view of the amygdala has been challenged. Studies of patients with amygdala lesions suggest that, whereas the amygdala is important for the identification of emotional facial expressions, it is not required for emotional experience (Anderson & Phelps, 2002). Furthermore, the amygdala is sensitive to novel and ambiguous stimuli as well as “emotional” stimuli per se (e.g., Whalen, 2007), and preferential amygdala activation for one stimulus category over another can be manipulated by shifting stimulus salience within the context of an experimental task (Cunningham, Van Bavel & Johnson, 2008). There is also recent evidence that the human amygdala plays an important role in regulation of social proximity, and may play a central role in mediating social interactions (Kennedy, Gläscher, Tyszka & Adolphs, 2009). Thus, cumulative evidence has led to the proposal that, rather than serving as a marker of emotional processing per se, the amygdala can be seen as a “motivational salience” or “biological relevance” detector important for the allocation of processing resources (Adolphs, 2008: Cunningham et al., 2008). Would characterizing amygdala activation as a marker of salience detection rather than as a signature of emotional processing change the interpretation of any of the literature reviewed?
These are all great points, but we felt that it would be very difficult to integrate them into the text without losing focus.
Second, it has been suggested that amygdala responses to rapidly presented or sub-attentive emotional faces has more to do with low-level featural characteristics of fearful or threatening faces — to visual salience — than to emotional salience related to signals of threat (Adolphs, 2008). In fact, there is evidence that preferential behavioral responses to fearful faces under conditions of limited attention may not rely on the amygdala. Tsuchiya, Moradi, Felsen et al. (2009) found that although SM, a woman with bilateral amygdala damage, could not explicity identify fearful expressions or discriminate their intensity, she showed a normal degree of prioritized processing of fearful faces when they were shown rapidly or at the threshold of awareness. Thus, although the amygdala may respond to crude featural differences that characterize fearful faces, such as exaggerated whites of the eyes, it may not be required for preferential behavioral discrimination of rapidly presented fearful faces. These findings, which are consistent with the view that the amygdala requires attention for discrimination of emotional – rather than visual – salience, could be included in the review.
Again, we were not able to discuss these issues here. But we very briefly touch upon them in the new opening paragraph.
A more minor point is that the Anderson et al. (2003) study is reported in this article as finding that amygdala responses to fear faces were not influenced by attentional load. However, the results of that study were somewhat more nuanced: Although amygdala activation in response to fearful faces was not reduced in low vs. high attention conditions, the amygdala failed to differentiate between fearful and disgusted faces in low-attention conditions. In contrast, in high attention conditions, amygdala activation was greater for fearful than disgust faces. This suggests that the amygdala makes very crude distinctions under conditions of low attention — again, possibly based on visual salience — and may require attention to discriminate emotional content [See 2.1 in text].
Valence
It is also important to at least briefly address the role of emotional valence on attention. The bulk of studies reviewed in this article used negative stimuli, including negative emotional expressions, fear conditioning, or images of mutilation. Although arousing positive stimuli effectively elicit amygdala activation (see meta-analysis by Sergerie et al., 2008), emotional valence may have an important effect on the relation between emotion and attention. A body of behavioral evidence suggests that whereas negative emotion narrows attentional and perceptual scope, positive emotion broadens it (e.g., Fredrickson & Branigan, 2005). In an fMRI study, Schmitz, de Rosa & Anderson (2009) showed images of faces surrounded by images of places in a task that required focus on the faces only. Following a positive mood induction, participants showed greater activation in a parahippocampal region selectively responsive to places (which were irrelevant to the task) than following a negative mood induction. This finding suggests that when participants were in a positive emotional state, more irrelevant place information was bleeding through the attentional filter imposed by the task, and that differently valenced emotional states can exert opposing influences on selective visual attention [See 2.2 in text].
Individual Differences in Attention
Finally, to account for discrepancies between experiments on the relative automaticity of emotional processing, this article raises the possibility that individual differences in “top-down” attention may contribute to conflicting results. This argument could be clarified and expanded [See 2.3 in text].
Reviewer C
A review regarding the insights gained by neuroscientific studies to the understanding of the attention-emotion relationship appears valuable and timely. A scholarly review is provided regarding the ‘automaticity’ of emotion processing. The author’s main emphasis regards effortlessness, a key feature of automaticity. Specifically, the question is addressed ‘Is emotion processing dependent on the availability of processing resources, or alternatively, resource independent?’. The focus of the review appears well-chosen as the issue has been addressed by a number of recent studies. Furthermore, other pertaining issues of the emotion-attention relationship received comparably less attention. I hope the authors find my comments and recommendations useful.
The authors provide a compelling case that the ‘priorized processing of emotional cues depends on the availability of processing resources. Importantly, this conclusion is based on converging evidence from fMRI- and ERP studies. Interestingly, a just-published study provides further support for this notion examining emotional stimuli presented in the peripheral field of vision (DeCesarei et al., 2009) [See 3.1 in text].
What I found is missing is a brief outline at the beginning of the review introducing the notion that emotion guides attention. The focus on priorization appears rather narrow. The extensive reference to experimental procedures is presumably most appealing to the expert. I found the writings of Lang and coworkers (1997) and Ohman and colleagues (2000) very helpful in this respect. Emotion is understood as action sets preparing responses. To prepare efficient actions, critical information from the environment needs to be extracted. In this sense, emotion guides attention.
Because emotion is such a multifaceted concept, we felt it would be difficult to include in the text a broader discussion of conceptual issues, for instance, some raised by the reviewer above. Nonetheless, we have briefly included a new first paragraph with some allusion to these issues. See 3.2 in the text.
The review would profit from introducing the notion of automaticity. For instance, in cognitive and social psychology, the concept of automaticity is discussed with respect to distinct key features. Is emotion processing obligatory, spontaneous, goal-dependent, resource-dependent, stimulus- driven, controllable? Furthermore, it has been suggested to examine each of the key features separately rather than treating automaticity as unitary construct (cf. Moors & De Hoewer, 2006). One possibility to deal with the issue is to briefly outline the (supporting) empirical evidence regarding several features of automaticity such as spontaneous, goal-indpeendent, stimulus-driven and resistant to habituation and highlight that capacity is the most critical feature regarding the automaticity of emotion processing [See 3.3 in text].
My main concerns regard the section ‘Attention is not required for emotional perception (again)’. The main message of the paragraph became not clear to me. Furthermore, I do not understand in which way the reported two studies support the conclusion ‘Whereas this framework can be used to explain a broad set of results, some findings appear to resist this explanation’. Considering the Schupp et al. study, it is examined whether visual emotion processing is modulated by task demands in the auditory modality. From the perspective of the Lavie-model, this research examined whether processing resources are shared among modalities, or are modality independent. In my reading, this finding refines the competition hypothesis rather than being inconsistent with it. Considering the Muller et al. study, the research examined the effect of emotional stimuli on the primary task stimuli rather than vice versa. The competition for processing resources among stimulus driven attention capture by emotion and top-down control by explicit task demands operates presumably in both directions. The Muller et al. (2008) findings provide empirical evidence for the bi-directional competition for processing resources.
We have attempted to clarify the issue of inter-modal competition and the implications of the findings of Shupp et al. [See 3.4 in text]. However, we disagree with the reviewer in what concerns the results by Muller et al. (2008). Our interpretation of their findings is that they are indeed problematic for accounts based on load, and that the results do challenge the notion of competition. We have tried to make these points clearer [See 3.5 in text].
In summary, the hypothesis that the priorized processing of emotional stimuli is resource-dependent seems well supported. The extent to which primary tasks interfere with emotion processing on the other hand seems to dependent on several variables. Strong emotional stimuli are more effective in attracting attention. More difficult tasks presumably engage a higher level of top-down control and focused attention on the task. Furthermore, the emotion-attention relationship may be highly context-specific as task characteristics (e.g. spatial vs. non-spatial tasks) greatly affect top-down regulation of the attentional focus. The issue is made even more complex when considering the temporal unfolding of stimulus processing. The relationship of emotion and attention may vary across processing stages and future studies may characterize the emotion-attention relationship in terms of interference at the level of fleeting processing stages in distinct neural regions.
