Seeing Positive: Positive Mood Enhances Visual Cortical EncodingBy Adam K. Anderson
Adam K. Anderson received his BS from Vassar College in Cognitive Science and his PhD in Experimental Psychology from Yale University, and completed postdoctoral training at Stanford University. He is a Canada Research Chair in Affective Neuroscience and Associate Professor in the Department of Psychology at the University of Toronto and a Research Associate at the Rotman Research Institute. His research focuses on the psychological and neural mechanisms of emotion-cognition interactions. In 2009 he was awarded the Ministry of Research and Innovation's Early Researcher Award and the American Psychological Association's Distinguished Scientific Award for Early Career Contribution to Psychology in Behavioral and Cognitive Neuroscience.
Seeing the world through rose-colored lenses may be less proverb and more empirical fact as converging evidence suggests that affective states are associated with changes in attention that may differentially affect perception and cognition. Affective states have long been argued to have potent interactions with cognition, shaping thought in opposing ways. Positive emotions have been linked to a creative and more generative mindset, and have been hypothesized to broaden one's thought-action repertoire, increasing the flexibility of cognition and its scope (Ashby, Isen, & Turken, 1999; Fredrickson, 2004; Isen, Daubman, & Nowicki, 1987; Rowe, Hirsh, & Anderson, 2007). By contrast, negative states are thought to induce the opposing tendency, engendering a more "functionally fixed" narrow mindset (Christianson, 1992; Derryberry & Tucker, 1994; Easterbrook, 1959). This distinction between flexible/broad versus rigid/narrow thinking styles associated with positive and negative states, respectively, has been found across diverse experimental and applied contexts, including intuitive judgments, decision making, creative problem solving tasks, and industrial negotiations.
A more far-reaching claim is that the valence of affective states influences not only the capacity for thinking but also perceiving (Fenske & Eastwood, 2003; Gable & Harmon-Jones, 2008; Gaspar & Clore, 2002; Rowe, Hirsh & Anderson, 2007). Attention regulates cognition to enable the control of thought, behavior, and perception. As such, altering the capacity for selective attention may not only have implications for internal conceptual processes but also the allocation of visuospatial attention to the external environment, shaping the initial process of perceptual encoding. Paralleling the effects on higher-level cognition, it has been hypothesized that the valence of affective states interacts with lower-level perceptual encoding in an opposing manner (Derryberry & Tucker, 1994; Rowe, Hirsh & Anderson, 2007), with positive affect broadening and negative affect narrowing attention. Although this is a matter of some debate (Gable and Harmon Jones 2008), positive versus negative mood is associated with greater global or holistic processing (i.e., the forest before the trees) versus local processing (i.e., the trees before the forest) (e.g., Basso, Schefft, Ris & Dember, 1996; Gaspar & Clore, 2002). However, rather than a genuine change in the scope of perceptual encoding, these behavioral data may originate in higher-level cognitive biases, where moods may increase or decrease access to what is in mind during the task at hand (Schwarz & Clore, 1983). In the case of global precedence, positive affect will further accentuate a bias towards global configurations. As such, the influence of affectively valenced states on the 'breadth' of visuospatial attention and perceptual encoding may serve more as a metaphorical description. A direct test of the field-of-view (FOV) hypothesis would examine whether positive and negative states exert opposing influences on attentional selection in the perceptual cortices. Evidential support for this hypothesis would demonstrate that endogenous emotional states influence the visual cortical encoding processes that underlie perception.
Behavioral (Eriksen & St James, 1986) and neuroimaging (Brefczynski & DeYoe, 1999) findings often ascribe selective visual attention the functionality of a spotlight-a mechanism for prioritizing information by narrowing or broadening cortical encoding of one's visual field-to suppress or enhance task irrelevant information processing. If valence-dependent states modulate visuospatial attentional breadth, then positive and negative states should have opposing influences on perceptual encoding of unattended stimuli in the periphery. Our first attempt at examining the FOV hypothesis used the flanker effect (Rowe, Hirsh & Anderson, 2007), whereby irrelevant flanker distractors are shown to influence a primary task (Eriksen & St James, 1986). We found that positive mood had a deleterious influence on spatial selective attention-impairing the ability to selectively focus on a target and thereby increased processing of spatially distant flanking distractors-consistent with expanded FOV. In fact, positive mood was as important in determining the size of flanker interference effect as flanker distance, indicated by an equivalent interference effect for far flankers under positive mood relative to near flankers under sad mood. That is, under positive mood, far flankers were processed as if they were physically near. An analysis of individual differences further revealed that greater flanker interference during positive mood was correlated with enhanced remote associates task performance, a task that requires finding unusual connections between a triad of words. These results demonstrate that positive affect exerts a common underlying influence on information processing, from external perceptual to internal conceptual attention. Consistent with the proposed function of positive affect, a buoyant mood may represent a fundamental shift in the "breadth" of information processing, represented by a decrease in the selectivity of attentional filters. The result of such a shift would be to cultivate a more open and exploratory mode of attention to both interoceptive and exteroceptive sources of information.
As a more direct test, we recently interrogated the FOV hypothesis with functional magnetic resonance imaging (fMRI) by alternating epochs of affect induction, where observers viewed mildly emotionally laden images (positive, neutral, and negative valence), with a simple visuospatial task (Schmitz, De Rosa & Anderson, 2009). Affect induction occurred independently from our measures of perceptual encoding, i.e., subjects were not simultaneously exposed to affective stimuli and the visuospatial task because it is known that emotionally arousing images alter activity in visual cortices. This design allowed us to independently assess the persisting effects of mood valence on perceptual encoding. In the visuospatial task, observers attended to a briefly presented (300 ms, to limit the role of eye movements) central neutral face presented with an unattended place in the peripheral surround (Figure 1). The visuospatial task capitalized on object-sensitive cortical processing of attended faces in the extrastriate fusiform face area (FFA) and unattended places in the parahippocampal place area (PPA) (Levy, Hasson, Avidan, Hendler & Malach, 2001). As face and place information were presented at different visual field locations, our physiological metric of FOV was a valence-dependent modulation of the PPA. Further, place stimuli were repeated to assess cortical adaptation (i.e., a reduction in brain activation associated with repetition of a stimulus), which is a neural index reflecting cortical memory for previously presented events. Rather than assuming magnitude of PPA response reflected place processing, this allowed us to more precisely index the encoding of specific places presented in the unattended surround.
Consistent with the FOV hypothesis, positive affective states increased and negative states decreased PPA response to novel places as well as cortical adaptation to repeated places (Figure 2). Furthermore, individual differences in self-reported positive and negative affect correlated inversely with PPA encoding of peripheral places. These results provide evidence that positive and negative affective states have opponent influences on visual cortical activity and encoding.
However, the extrastriate PPA findings represent a relatively late non-retinotopically organized stage of visual selection, and thus do not demonstrate that affective influences extend to the earliest stages of visual cortical processing that would support changes in FOV. To better appreciate the cortical pathways involved in gating PPA response, we additionally employed psycho-physiological interaction analyses to interrogate how positive and negative states differentially modulated functional coupling between the PPA and distal neuronal populations. These analyses demonstrated that affective valence modulated the relationship between the earliest stages of visual cortex along the calcarine sulcus (primary visual cortex, PVC) and later higher order stages of object encoding in the inferior temporal cortex (PPA). Specifically, positive affect may increase the propagation of peripheral information to higher order regions of the brain. By contrast, negative affect may decrease this propagation. These findings collectively suggest positive states decrease and negative states increase the filtering of unattended peripheral information. Thus, positive and negative affective states exerted opposing influences on the informational bandwidth of perceptual encoding, altering the FOV or scope of the proverbial 'attentional spotlight'.
This work demonstrates that opposing effects of affective states are not restricted to later influences on higher-order thinking and reasoning, but extend to earlier stages of selection in the perceptual cortices, biasing the course of perceptual encoding. These valence-dependent interactions with inferior temporal visual cortices observed during our visuospatial task occurred in the absence of external affective cues, and, despite the fact that both the cognitive and perceptual features of all visuospatial task blocks were equated. As such, we demonstrate that endogenous affective states themselves are capable of influencing visual cortical processing. Internal affective states therefore fundamentally bias the visual cortical lens through which external perceptual experience is filtered, increasing versus decreasing FOV.
As positive versus negative states have been associated with heuristic versus analytic modes of cognitive processing (Schwarz & Clore, 1988), they may differ in the effortful top-down recruitment of attentional networks, resulting in more versus less central task engagement. This may account for more or less processing of the unattended surround. The behavioral and brain data related to central face processing did not reveal such a tradeoff in performance under positive relative to negative states, and thus do not support such a motivational account. Moreover, our results suggest affective states modulate perceptual encoding via altered coupling with posterior sensory cortices as opposed to a more indirect top-down influence via altered engagement of attentional networks. Rather than engaging attention more or less, positive and negative states may have a more fundamental influence on the processing dynamics between primary, secondary and higher associative cortices. A better understanding of these putative valence-specific processing modes may be gleaned from brain regions associated with the generation of positive and negative states. Valence-specific patterns of brain response were found during negative and positive affect induction, respectively, in the amygdala and medial orbitofrontal cortex (mOFC), which were sustained during the interleaved visuospatial task. Additionally, self-reported valence ratings correlated inversely with the amygdala and mOFC as well as with peripheral visual processing as indexed by place encoding in the PPA. Thus, neural activity in these affective substrates may represent neural states associated with mood that bias sensitivity to perceptual inputs.
Although the amygdala has been associated with both positive and negative affect (Anderson & Sobel, 2003), it is also modulated by evaluative goals and may support an attentional negativity bias (Cunningham, Van Bavel, & Johnsen, 2008). Consistent with a narrow attentional processing mode, the amygdala has been shown to support vigilance towards negatively arousing relative to other sensory events competing for processing resources (Anderson & Phelps, 2001), and increased selectivity (i.e. tuning) of the sensory cortices following fear conditioning (Morris, Friston & Dolan, 1998). Further, amygdala responses correlate with extrastriate response during negative image processing predicting later enhanced memory specifically for image details (Kensinger, Garoff-Eaton, & Schacter, 2007). Rather than attributing our valence-dependent amygdala finding to the emergence of a negative affective state, we propose instead that the amygdala may facilitate a specific mode of sensory information processing with a narrow FOV as a perceptual correlate, triggered by negative and possibly also by high motivation positive states (Gable and Harmon-Jones, 2008). As such, amygdalar inputs may bias a more circumscribed feed-forward processing from posterior structures, hypothetically yielding a more selective propagation of sensory information.
By contrast, neural theories of the influence of positive affect on cognition highlight the role of mesocortical dopamine systems on inhibitory and cognitive control (Ashby, Isen, & Turken, 1999), which is thought to facilitate switches in attentional set and perspective. Indeed, we found that self-reported positive affect correlated with sustained activation of a mesocortical target region in the mOFC, a region in which reward-related processing may extend to include more exploratory modes of thought and behavior (Daw, O'Dherty, Dayan, Seymour, & Dolan, 2006), such as suboptimal exploratory selections in an incentive learning gambling task, improvisation, and insightful problem solving (Subramaniam, Kounios, Parrish, & Jung-Beeman, 2008) This neuroimaging evidence complements a long line of behavioral research linking positive emotion with increased scope and flexibility of cognition. Cortical disinhibition may extend to attentional control over earlier perceptual processes, enhancing processing from posterior perceptual regions. This would yield a less selective propagation of sensory information. The present findings suggest the influence of affective states may extend beyond high-level cognition to earlier stages of perceptual processing, resulting in a more exploratory and global analysis of perceptual inputs.
In sum, these new data provide evidence that internal affective states alter visual cortical processing in a valence-dependent manner, with positive affect increasing and negative affect decreasing the bandwidth or FOV of perceptual encoding. The origins of these opposing valence-dependent influences may arise from more primitive opposing action tendencies supported by subcortical structures, such as the amygdala, to enhance stereotyped defensive reflexes (Davis & Whalen, 2001) and mesocortical prefrontal regions that enhance novel or exploratory appetitive behavior (Daw et al., 2006). In combination, these neural systems may represent a fundamental underlying bias on neural dynamics supporting information processing, where altered scope of internal conceptual processes supporting thought may originate from altered scope of perceptual encoding of the external environment (Rowe, Hirsh, & Anderson 2007). As such, the rose-colored lenses of a good mood may have less to do with the color and more to with the expansiveness of the view.
Anderson, A. K. & Phelps, E. A. (2001). Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature, 411(6835), 305-309.
Anderson, A. K. & Sobel, N. (2003). Dissociating intensity from valence as sensory inputs to emotion. Neuron, 39(4), 581-583.
Ashby, F. G., Isen, A. M., & Turken, A. U. (1999). A neuropsychological theory of positive affect and its influence on cognition. Psychological Review, 106(3), 529-550.
Basso, M. R., Schefft, B. K., Ris, M. D., & Dember, W. N. (1996). Mood and global-local visual processing. Journal of the International Neuropsychological Society, 2(3), 249-255.
Brefczynski, J. A. & DeYoe, E. A. (1999). A physiological correlate of the 'spotlight' of visual attention. Nature Neuroscience, 2(4), 370-374.
Christianson, S. A. (1992). Emotional stress and eyewitness memory: a critical review. Psychological Bulletin, 112, 284-309.
Cunningham, W. A., Van Bavel, J. J., & Johnsen, I. R. (2008). Affective flexibility: evaluative processing goals shape amygdala activity. Psychological Science, 19(2), 152-160.
Davis, M. & Whalen, P. J. (2001). The amygdala: vigilance and emotion. Molecular Psychiatry, 6(1), 13-34.
Daw, N. D., O'Doherty, J. P., Dayan, P., Seymour, B., & Dolan, R. J. (2006). Cortical substrates for exploratory decisions in humans. Nature, 441(7095), 876-879.
Derryberry, D., & Tucker, D. M. (1994). Motivating the focus of attention. In P. M. Niedenthal & S. Kitayama (Eds), The heart's eye: Emotional influences in perception and attention (pp.167-196), San Diego, California: Academic Press.
Dreisbach, G. (2006). How positive affect modulates cognitive control: The costs and benefits of reduced maintenance capability. Brain and Cognition, 60(1), 11-19.
Easterbrook, J. A. (1959). The effect of emotion on cue utilization and the organization of behavior. Psychological Review, 66, 183-201.
Eriksen, C. W. & St James, J. D. (1986). Visual attention within and around the field of focal attention: A zoom lens model. Perception & Psychophysics, 40(4), 225-240.
Fenske, M. J. & Eastwood, J. D. (2003). Modulation of focused attention by faces expressing emotion: Evidence from flanker tasks. Emotion, 3(4), 327-343.
Fredrickson, B. L. (2004). The broaden-and-build theory of positive emotions. Philosophical transactions of the Royal Society of London, 359(1449), 1367-1378.
Gable, P. A. & Harmon-Jones, E. (2008). Approach-motivated positive affect reduces breadth of attention. Psychological Science, 19(5), 476-482.
Gasper, K. & Clore, G. L. (2002). Attending to the big picture: mood and global versus local processing of visual information. Psychological Science, 13(1), 34-40.
Isen, A. M., Daubman, K. A., & Nowicki, G. P. (1987). Positive affect facilitates creative problem solving. Journal of Personality and Social Psychology, 52(6), 1122-1131.
Kensinger, E. A., Garoff-Eaton, R. J., & Schacter, D. L. (2007). How negative emotion enhances the visual specificity of a memory. Journal of Cognitive Neuroscience, 19(11), 1872-1887.
Levy, I., Hasson, U., Avidan, G., Hendler, T., & Malach, R. (2001). Center-periphery organization of human object areas. Nature Neuroscience, 4(5), 533-539.
Morris, J. S., Friston, K. J., & Dolan, R. J. (1998). Experience-dependent modulation of tonotopic neural responses in human auditory cortex. Proceedings of the Royal Society: Biological Sciences, 265(1397), 649-657.
Rowe, G., Hirsh, J. B., & Anderson, A. K. (2007). Positive affect increases the breadth of attentional selection. Proceedings of the National Academy of Sciences of the United States of America, 104(1), 383-388.
Schmitz, T. W., De Rosa, E., & Anderson, A. K. (2009). Opposing influences of affective state valence on visual cortical encoding. Journal of Neuroscience, 3;29(22), 7199-207
Schwarz, N. & Clore, G. L. (1983). Mood, misattribution, and judgments of well-being: Informative and directive functions of affective states. Journal of Personality and Social Psychology, 45(3), 513-523.
Schwarz, N. & Clore, G. L. (1988). How do I feel about it? The information function of affective states. In K. Fiedler, and J. Forgas (Eds), Affect, cognition and social behavior: New evidence and integrative attempts. Toronto: C.J. Hogrefe.
Subramaniam, K., Kounios, J., Parrish, T. B., & Jung-Beeman, M. (2008). A brain mechanism for facilitation of insight by positive affect. Journal of Cognitive Neuroscience, 21(3), 415-432.