Abstract
A huge amount of environmental stimulus input constantly enters the brain via the different sensory channels of the organism. Due to its limited capacity, the brain cannot process all the inputs exhaustively, and thus needs to select a subset of stimuli for further processing at the cost of others. Emotional stimuli, for example social signals such as angry faces or happy voices, are privileged in the competition for attentional processing resources: the neural representation of emotional stimuli is stronger and more robust compared to neutral stimuli; emotional stimuli are prioritized in perception, draw attention more quickly, and impede attentional disengagement longer than neutral stimuli. The representations of emotional stimuli are thus intensified at different stages of processing. This generates a vivid conscious percept allowing organisms to prepare and implement adequate responses. By modulating frontoparietal attention systems, emotional stimuli also impact on the perceptual processing of subsequent stimuli appearing at the same location as an emotional stimulus. Such neurocognitive selection mechanisms thus drastically reorganize our representation and perception of the environment by focusing on emotionally and motivationally relevant events and their immediate spatial and temporal periphery.
Until now, the effects of emotional stimuli on attentional processes have mainly been described within a sensory modality, most frequently using pictures of emotional stimuli to modulate visuospatial attention. However, in real-life situations humans typically encounter simultaneous input to several different senses, such as vision, audition, olfaction, and touch. Signals entering these different channels might originate from a common, emotionally relevant source. To receive maximal benefit from multimodal sensory input, the brain must coordinate the input appropriately so that signals from a relevant common source are rapidly processed and integrated across the different input channels to allow for the preparation and implementation of adaptive responses.
We review the current evidence for cross-modal modulation of spatial attention by emotional information. Presenting data from behavioral and electrophysiological investigations in human subjects we illustrate, for example, the effects of emotional voices on visual attention and the effects of emotional images on haptic attention. The data converge to show that emotion modulates attentional processing across sensory modalities by boosting early sensory stages of processing, potentially implemented by a large-scale neural network centered around the amygdala, providing direct and indirect top-down signals to sensory pathways and frontoparietal pathways involved in exogenous and endogenous attentional selection processes.
This rapid cross-modal integration at multiple stages of processing may reflect a fundamental principle of human brain organization: to prioritize the processing of emotionally relevant stimuli, even if they are outside the focus of spatial attention, thus facilitating the multimodal assessment of emotionally relevant stimuli in the environment.
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References
Amaral, D. G., Behniea, H., & Kelly, J. L. (2003). Topographic organization of projections from the amygdala to the visual cortex in the macaque monkey. Neuroscience, 118, 1099–1120.
Andersen, R. A., Snyder, L. H., Bradley, D. C., & Xing, J. (1997). Multimodal representation of space in the posterior parietal cortex and its use in planning movements. Annual Review of Neuroscience, 20, 303–330.
Anderson, A. K., & Phelps, E. A. (2001). Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature, 411, 305–309.
Bertels, J., Kolinsky, R., & Morais, J. (2010). Emotional valence of spoken words influences the spatial orienting of attention. Acta Psychologica, 134, 264–278.
Bishop, S. J., Duncan, J., Brett, M., & Lawrence, A. D. (2004). Prefrontal cortical function and anxiety: Controlling attention to threat-related stimuli. Nature Neuroscience, 7, 184–188.
Brosch, T., Grandjean, D., Sander, D., & Scherer, K. R. (2008). Behold the voice of wrath: Cross-modal modulation of visual attention by anger prosody. Cognition, 106, 1497–1503.
Brosch, T., Grandjean, D., Sander, D., & Scherer, K. R. (2009). Cross-modal emotional attention: Emotional voices modulate early stages of visual processing. Journal of Cognitive Neuroscience, 21, 1670–1679.
Brosch, T., Sander, D., Pourtois, G., & Scherer, K. R. (2008). Beyond fear: Rapid spatial orienting towards positive emotional stimuli. Psychological Science, 19, 362–370.
Brosch, T., Sander, D., & Scherer, K. R. (2007). That baby caught my eye… Attention capture by infant faces. Emotion, 7, 685–689.
Brosch, T., Pourtois, G., Sander, D., & Vuilleumier, P. (2011). Additive effects of emotional, endogenous, and exogenous attention: behavioral and electrophysiological evidence. Neuropsychologia, 49(7), 1779–1787.
Campanella, S., & Belin, P. (2007). Integrating face and voice in person perception. Trends in Cognitive Sciences, 11, 535–543.
Carrasco, M., Ling, S., & Read, S. (2004). Attention alters appearance. Nature Neuroscience, 7, 308–313.
Cerf, M., Thiruvengadam, N., Mormann, F., Kraskov, A., Quiroga, R. Q., Koch, C., et al. (2010). On-line, voluntary control of human temporal lobe neurons. Nature, 467, 1104–1108.
Corbetta, M., Patel, G., & Shulman, G. L. (2008). The reorienting system of the human brain: From environment to theory of mind. Neuron, 58, 306–324.
Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3, 201–215.
Desimone, R., & Duncan, J. (1995). Neural mechanisms of selective visual attention. Annual Review of Neuroscience, 18, 193–222.
Dolan, R. J., Morris, J. S., & de Gelder, B. (2001). Crossmodal binding of fear in voice and face. Proceedings of the National Academy of Sciences of the United States of America, 98, 10006–10010.
Dowman, R. (2007). Neural mechanisms of detecting and orienting attention toward unattended threatening somatosensory targets. I. Intermodal effects. Psychophysiology, 44, 407–419.
Dowman, R., & Ben-Avraham, D. (2008). An artificial neural network model of orienting attention toward threatening somatosensory stimuli. Psychophysiology, 45, 229–239.
Driver, J. (2001). A selective review of selective attention research from the past century. British Journal of Psychology, 92, 53–78.
Driver, J., & Spence, C. (1998). Crossmodal attention. Current Opinion in Neurobiology, 8, 245–253.
Egeth, H. E., & Yantis, S. (1997). Visual attention: Control, representation, and time course. Annual Review of Psychology, 48, 269–297.
Eimer, M., Cockburn, D., Smedley, B., & Driver, J. (2001). Cross-modal links in endogenous spatial attention are mediated by common external locations: Evidence from event-related brain potentials. Experimental Brain Research, 139, 398–411.
Eimer, M., & Driver, J. (2001). Crossmodal links in endogenous and exogenous spatial attention: Evidence from event-related brain potential studies. Neuroscience and Biobehavioral Reviews, 25, 497–511.
Eimer, M., & Holmes, A. (2007). Event-related brain potential correlates of emotional face processing. Neuropsychologia, 45, 15–31.
Ethofer, T., Anders, S., Erb, M., Droll, C., Royen, L., Saur, R., et al. (2006). Impact of voice on emotional judgment of faces: An event-related fMRI study. Human Brain Mapping, 27, 707–714.
Ethofer, T., Anders, S., Wiethoff, S., Erb, M., Herbert, C., Saur, R., et al. (2006). Effects of prosodic emotional intensity on activation of associative auditory cortex. Neuroreport, 17, 249–253.
Grandjean, D., Bänziger, T., & Scherer, K. R. (2006). Intonation as an interface between language and affect. Progress in Brain Research, 156, 235–247.
Grandjean, D., Sander, D., Lucas, N., Scherer, K. R., & Vuilleumier, P. (2008). Effects of emotional prosody on auditory extinction for voices in patients with spatial neglect. Neuropsychologia, 46, 487–496.
Grandjean, D., Sander, D., Pourtois, G., Schwartz, S., Seghier, M. L., Scherer, K. R., et al. (2005). The voices of wrath: Brain responses to angry prosody in meaningless speech. Nature Neuroscience, 8, 145–146.
Hein, G., & Knight, R. T. (2008). Superior temporal sulcus—It’s my area: Or is it? Journal of Cognitive Neuroscience, 20, 2125–2136.
Hillyard, S. A., Vogel, E. K., & Luck, S. J. (1998). Sensory gain control (amplification) as a mechanism of selective attention: Electrophysiological and neuroimaging evidence. Philosophical Transactions of the Royal Society B: Biological Sciences, 353, 1257–1270.
Keil, A., Bradley, M. M., Junghofer, M., Russmann, T., Lowenthal, W., & Lang, P. J. (2007). Cross-modal attention capture by affective stimuli: Evidence from event-related potentials. Cognitive Affective and Behavioral Neuroscience, 7, 18–24.
Kennett, S., Eimer, M., Spence, C., & Driver, J. (2001). Tactile-visual links in exogenous spatial attention under different postures: Convergent evidence from psychophysics and ERPs. Journal of Cognitive Neuroscience, 13, 462–478.
Koelewijn, T., Bronkhorst, A., & Theeuwes, J. (2010). Attention and the multiple stages of multisensory integration: A review of audiovisual studies. Acta Psychologica, 134, 372–384.
Kreifelts, B., Ethofer, T., Shiozawa, T., Grodd, W., & Wildgruber, D. (2009). Cerebral representation of non-verbal emotional perception: fMRI reveals audiovisual integration area between voice- and face-sensitive regions in the superior temporal sulcus. Neuropsychologia, 47, 3059–3066.
LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23, 155–184.
Lipp, O. V., & Derakshan, N. (2005). Attentional bias to pictures of fear-relevant animals in a dot probe task. Emotion, 5, 365–369.
Lloyd, D. M., Bolanowski, S. J., Jr., Howard, L., & McGlone, F. (1999). Mechanisms of attention in touch. Somatosensory and Motor Research, 16, 3–10.
MacLeod, C., Mathews, A., & Tata, P. (1986). Attentional bias in emotional disorders. Journal of Abnormal Psychology, 95, 15–20.
Marois, R., & Ivanoff, J. (2005). Capacity limits of information processing in the brain. Trends in Cognitive Sciences, 9, 296–305.
McDonald, J. J., Teder-Salejarvi, W. A., Di Russo, F., & Hillyard, S. A. (2003). Neural substrates of perceptual enhancement by cross-modal spatial attention. Journal of Cognitive Neuroscience, 15, 10–19.
Miles, E., Poliakoff, E., & Brown, R. J. (2008). Investigating the time course of tactile reflexive attention using a non-spatial discrimination task. Acta Psychologica, 128, 210–215.
Mohanty, A., Egner, T., Monti, J. M., & Mesulam, M. M. (2009). Search for a threatening target triggers limbic guidance of spatial attention. Journal of Neuroscience, 29, 10563–10572.
Ohman, A., Flykt, A., & Esteves, F. (2001). Emotion drives attention: Detecting the snake in the grass. Journal of Experimental Psychology: General, 130, 466–478.
Olofsson, J. K., Nordin, S., Sequeira, H., & Polich, J. (2008). Affective picture processing: An integrative review of ERP findings. Biological Psychology, 77, 247–265.
Peelen, M., Atkinson, A., Andersson, F., & Vuilleumier, P. (2007). Emotional modulation of body-selective visual areas. Social Cognitive and Affective Neuroscience, 2, 274–283.
Peelen, M., Heslenfeld, D. J., & Theeuwes, J. (2004). Endogenous and exogenous attention shifts are mediated by the same large-scale neural network. Neuroimage, 22, 822–830.
Penfield, W., & Rasmussen, T. (1950). The cerebral cortex of man. New York, NY: Macmillan.
Phelps, E. A. (2006). Emotion and cognition: Insights from studies of the human amygdala. Annual Review of Psychology, 57, 27–53.
Phelps, E. A., Ling, S., & Carrasco, M. (2006). Emotion facilitates perception and potentiates the perceptual benefits of attention. Psychological Science, 17, 292–299.
Poliakoff, E., Miles, E., Li, X., & Blanchette, I. (2007). The effect of visual threat on spatial attention to touch. Cognition, 102, 405–414.
Posner, M. I. (1980). Orienting of attention. Quarterly Journal of Experimental Psychology, 32, 3–25.
Posner, M. I., Snyder, C. R., & Davidson, B. J. (1980). Attention and the detection of signals. Journal of Experimental Psychology, 109, 160–174.
Pourtois, G., Grandjean, D., Sander, D., & Vuilleumier, P. (2004). Electrophysiological correlates of rapid spatial orienting towards fearful faces. Cerebral Cortex, 14, 619–633.
Pourtois, G., Schwartz, S., Seghier, M. L., Lazeyras, F., & Vuilleumier, P. (2006). Neural systems for orienting attention to the location of threat signals: An event-related fMRI study. Neuroimage, 31, 920–933.
Pourtois, G., Thut, G., Grave de Peralta, R., Michel, C., & Vuilleumier, P. (2005). Two electrophysiological stages of spatial orienting towards fearful faces: Early temporo-parietal activation preceding gain control in extrastriate visual cortex. Neuroimage, 26, 149–163.
Rinck, M., Reinecke, A., Ellwart, T., Heuer, K., & Becker, E. S. (2005). Speeded detection and increased distraction in fear of spiders: Evidence from eye movements. Journal of Abnormal Psychology, 114, 235–248.
Rossi, A. F., & Paradiso, M. A. (1995). Feature-specific effects of selective visual attention. Vision Research, 35, 621–634.
Sander, D., Grafman, J., & Zalla, T. (2003). The human amygdala: An evolved system for relevance detection. Reviews in the Neurosciences, 14, 303–316.
Sander, D., Grandjean, D., Pourtois, G., Schwartz, S., Seghier, M. L., Scherer, K. R., et al. (2005). Emotion and attention interactions in social cognition: Brain regions involved in processing anger prosody. Neuroimage, 28, 848–858.
Sander, K., & Scheich, H. (2001). Auditory perception of laughing and crying activates human amygdala regardless of attentional state. Cognitive Brain Research, 12, 181–198.
Scherer, K. R. (2001). Appraisal considered as a process of multilevel sequential checking. In K. R. Scherer, A. Schorr, & T. Johnstone (Eds.), Appraisal processes in emotion: Theory, methods, research (pp. 92–120). New York, NY: Oxford University Press.
Schirmer, A., Teh, K. S., Wang, S., Vijayakumar, R., Ching, A., Nithianantham, D., Escoffier, N., Cheok, A.D. (2011). Squeeze me, but don’t tease me: human and mechanical touch enhance visual attention and emotion discrimination. Social Neuroscience, 6(3), 219–230.
Smith, S. D., Most, S. B., Newsome, L. A., & Zald, D. H. (2006). An emotion-induced attentional blink elicited by aversively conditioned stimuli. Emotion, 6, 523–527.
Spence, C. (2010). Crossmodal spatial attention. Annals of the New York Academy of Science, 1191, 182–200.
Spence, C., & Driver, J. (1994). Covert spatial orienting in audition: Exogenous and endogenous mechanisms facilitate sound localization. Journal of Experimental Psychology-Human Perception and Performance, 20, 555–574.
Stein, B. E., & Stanford, T. R. (2008). Multisensory integration: Current issues from the perspective of the single neuron. Nature Reviews Neuroscience, 9, 255–266.
Theeuwes, J. (1991). Exogenous and endogenous control of attention: The effect of visual onsets and offsets. Perception and Psychophysics, 49, 83–90.
Turatto, M., Mazza, V., & Umilta, C. (2005). Crossmodal object-based attention: Auditory objects affect visual processing. Cognition, 96, B55–B64.
Van Damme, S., Gallace, A., Spence, C., Crombez, G., & Moseley, G. L. (2009). Does the sight of physical threat induce a tactile processing bias? Modality-specific attentional facilitation induced by viewing threatening pictures. Brain Research, 1253, 100–106.
von Kriegstein, K., Kleinschmidt, A., Sterzer, P., & Giraud, A. L. (2005). Interaction of face and voice areas during speaker recognition. Journal of Cognitive Neuroscience, 17, 367–376.
Vuilleumier, P. (2005). How brains beware: Neural mechanisms of emotional attention. Trends in Cognitive Sciences, 9, 585–594.
Vuilleumier, P., Armony, J. L., Driver, J., & Dolan, R. J. (2001). Effects of attention and emotion on face processing in the human brain: An event-related fMRI study. Neuron, 30, 829–841.
Vuilleumier, P., & Brosch, T. (2009). Interactions of emotion and attention. In M. S. Gazzaniga (Ed.), The cognitive neurosciences IV (pp. 925–934). Cambridge, MA: MIT Press.
Vuilleumier, P., & Pourtois, G. (2007). Distributed and interactive brain mechanisms during emotion face perception: Evidence from functional neuroimaging. Neuropsychologia, 45, 174–194.
Vuilleumier, P., & Schwartz, S. (2001). Beware and be aware: Capture of spatial attention by fear-related stimuli in neglect. Neuroreport, 12, 1119–1122.
West, G. L., Anderson, A. A., Ferber, S., & Pratt, J. (2011). Electrophysiological evidence for biased competition in V1 for fear expressions. Journal of Cognitive Neuroscience, 23(11), 3410–3418.
West, G. L., Anderson, A. A., & Pratt, J. (2009). Motivationally significant stimuli show visual prior entry: Evidence for attentional capture. Journal of Experimental Psychology-Human Perception and Performance, 35, 1032–1042.
Whalen, P. J., Rauch, S. L., Etcoff, N. L., McInerney, S. C., Lee, M. B., & Jenike, M. A. (1998). Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. Journal of Neuroscience, 18, 411–418.
Wolfe, J. M., & Horowitz, T. S. (2004). What attributes guide the deployment of visual attention and how do they do it? Nature Reviews Neuroscience, 5, 495–501.
Yantis, S. (1992). Multielement visual tracking: Attention and perceptual organization. Cognitive Psychology, 24, 295–340.
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Brosch, T., Grandjean, D. (2013). Cross-Modal Modulation of Spatial Attention by Emotion. In: Belin, P., Campanella, S., Ethofer, T. (eds) Integrating Face and Voice in Person Perception. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-3585-3_11
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