Abstract
A subcortical pathway through the superior colliculus and pulvinar to the amygdala is commonly assumed to mediate the non-conscious processing of affective visual stimuli. We review anatomical and physiological data that argue against the notion that such a pathway plays a prominent part in processing affective visual stimuli in humans. Instead, we propose that the primary role of the amygdala in visual processing, like that of the pulvinar, is to coordinate the function of cortical networks during evaluation of the biological significance of affective visual stimuli. Under this revised framework, the cortex has a more important role in emotion processing than is traditionally assumed.
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References
Tamietto, M. & de Gelder, B. Neural bases of the non-conscious perception of emotional signals. Nature Rev. Neurosci. 11, 697–709 (2010).
Ohman, A. & Mineka, S. Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. Psychol. Rev. 108, 483–522 (2001).
Lonsdorf, T. B. et al. Genetic gating of human fear learning and extinction: possible implications for gene–environment interaction in anxiety disorder. Psychol. Sci. 20, 198–206 (2009).
LeDoux, J. E. The Emotional Brain (Simon & Schuster, New York, 1996).
Dolan, R. J. & Vuilleumier, P. Amygdala automaticity in emotional processing. Ann. NY Acad. Sci. 985, 348–355 (2003).
Ohman, A., Lundqvist, D. & Esteves, F. The face in the crowd revisited: a threat advantage with schematic stimuli. J. Pers. Soc. Psychol. 80, 381–396 (2001).
Yang, E., Zald, D. H. & Blake, R. Fearful expressions gain preferential access to awareness during continuous flash suppression. Emotion 7, 882–886 (2007).
Morris, J. S., Ohman, A. & Dolan, R. J. Conscious and unconscious emotional learning in the human amygdala. Nature 393, 467–470 (1998).
Whalen, P. J. et al. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J. Neurosci. 18, 411–418 (1998).
Morris, J. S., DeGelder, B., Weiskrantz, L. & Dolan, R. J. Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. Brain 124, 1241–1252 (2001).
Pegna, A. J., Khateb, A., Lazeyras, F. & Seghier, M. L. Discriminating emotional faces without primary visual cortices involves the right amygdala. Nature Neurosci. 8, 24–25 (2005).
Morris, J. S., Ohman, A. & Dolan, R. J. A subcortical pathway to the right amygdala mediating “unseen” fear. Proc. Natl Acad. Sci. USA 96, 1680–1685 (1999).
Bar, M. & Neta, M. Humans prefer curved visual objects. Psychol. Sci. 17, 645–648 (2006).
Vuilleumier, P., Armony, J. L., Driver, J. & Dolan, R. J. Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nature Neurosci. 6, 624–631 (2003).
Davis, M. & Whalen, P. J. The amygdala: vigilance and emotion. Mol. Psychiatry 6, 13–34 (2001).
Whalen, P. J. & Phelps, E. A. (eds) The Human Amygdala (Guilford Press, New York, 2009).
Lewis, M. D. Bridging emotion theory and neurobiology through dynamic systems modeling. Behav. Brain Sci. 28, 169–245 (2005).
Duncan, S. & Barrett, L. F. Affect is a form of cognition: a neurobiological analysis. Cogn. Emot. 21, 1184–1211 (2007).
Pessoa, L. On the relationship between emotion and cognition. Nature Rev. Neurosci. 9, 148–158 (2008).
Pessoa, L. To what extent are emotional visual stimuli processed without attention and awareness? Curr. Opin. Neurobiol. 15, 188–196 (2005).
Adolphs, R. Fear, faces, and the human amygdala. Curr. Opin. Neurobiol. 18, 166–172 (2008).
Pizzagalli, D., Regard, M. & Lehmann, D. Rapid emotional face processing in the human right and left brain hemispheres: an ERP study. Neuroreport 10, 2691–2698 (1999).
Halgren, E., Raij, T., Marinkovic, K., Jousmaki, V. & Hari, R. Cognitive response profile of the human fusiform face area as determined by MEG. Cereb. Cortex 10, 69–81 (2000).
Eger, E., Jedynak, A., Iwaki, T. & Skrandies, W. Rapid extraction of emotional expression: evidence from evoked potential fields during brief presentation of face stimuli. Neuropsychologia 41, 808–817 (2003).
Japee, S., Crocker, L., Carver, F., Pessoa, L. & Ungerleider, L. G. Individual differences in valence modulation of face-selective M170 response. Emotion 9, 59–69 (2009).
Krolak-Salmon, P., Henaff, M. A., Vighetto, A., Bertrand, O. & Mauguiere, F. Early amygdala reaction to fear spreading in occipital, temporal, and frontal cortex: a depth electrode ERP study in human. Neuron 42, 665–676 (2004).
Greene, M. R. & Oliva, A. The briefest of glances: the time course of natural scene understanding. Psychol. Sci. 20, 464–472 (2009).
Kawasaki, H. et al. Single-neuron responses to emotional visual stimuli recorded in human ventral prefrontal cortex. Nature Neurosci. 4, 15–16 (2001).
Amaral, D. G., Price, J. L., Pitkanen, A. & Carmichael, S. T. in The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction (ed. Aggleton, J.) 1–66 (Wiley-Liss, New York, 1992).
Gothard, K. M., Battaglia, F. P., Erickson, C. A., Spitler, K. M. & Amaral, D. G. Neural responses to facial expression and face identity in the monkey amygdala. J. Neurophysiol. 97, 1671–1683 (2007).
Rolls, E. T. Emotion Explained (Oxford Univ. Press, Oxford, 2005).
Kreiman, G., Koch, C. & Fried, I. Category-specific visual responses of single neurons in the human medial temporal lobe. Nature Neurosci. 3, 946–953 (2000).
Mormann, F. et al. Latency and selectivity of single neurons indicate hierarchical processing in the human medial temporal lobe. J. Neurosci. 28, 8865–8872 (2008).
Smith, M. L., Cottrell, G. W., Gosselin, F. & Schyns, P. G. Transmitting and decoding facial expressions. Psychol. Sci. 16, 184–189 (2005).
Smith, F. W. & Schyns, P. G. Smile through your fear and sadness: transmitting and identifying facial expression signals over a range of viewing distances. Psychol. Sci. 20, 1202–1208 (2009).
Adolphs, R. et al. A mechanism for impaired fear recognition after amygdala damage. Nature 433, 68–72 (2005).
Vuilleumier, P. How brains beware: neural mechanisms of emotional attention. Trends Cogn. Sci. 9, 585–594 (2005).
Pessoa, L., Oliveira, L. & Pereira, M. G. Attention and emotion. Scholarpedia 5, 6314 (2010).
Pessoa, L., Oliveira, L. & Pereira, M. G. in Handbook of Human Affective Neuroscience (eds Armony, J. L. & Vuilleumier, P.) (Cambridge Univ. Press, Cambridge, UK, 2011).
Tsuchiya, N., Moradi, F., Felsen, C., Yamazaki, M. & Adolphs, R. Intact rapid detection of fearful faces in the absence of the amygdala. Nature Neurosci. 12, 1224–1225 (2009).
Piech, R. M. et al. Fear-enhanced visual search persists after amygdala lesions. Neuropsychologia. 48, 3430–3435 (2010).
Grieve, K. L., Acuna, C. & Cudeiro, J. The primate pulvinar nuclei: vision and action. Trends Neurosci. 23, 35–39 (2000).
Stepniewska, I. in The Primate Visual System (eds Kaas, J. & Collins, C. E.) 53–80 (CRC Press, Boca Raton, Florida, 2004).
Bender, D. B. Visual activation of neurons in the primate pulvinar depends on cortex but not colliculus. Brain Res. 279, 258–261 (1983).
Robinson, D. L. & Cowie, R. J. in The Thalamus (ed. McCormick, D.) 53–92 (Elsevier, New York, 1997).
de Gelder, B. et al. Standing up for the body. Recent progress in uncovering the networks involved in the perception of bodies and bodily expressions. Neurosci. Biobehav. Rev. 34, 513–527 (2010).
Guillery, R. W. Anatomical evidence concerning the role of the thalamus in corticocortical communication: a brief review. J. Anat. 187, 583–592 (1995).
Sherman, S. M. & Guillery, R. W. Functional organization of thalamocortical relays. J. Neurophysiol. 76, 1367–1395 (1996).
Sherman, S. M. Thalamus. Scholarpedia 1, 1583 (2006).
Ungerleider, L. G. & Christensen, C. A. Pulvinar lesions in monkeys produce abnormal scanning of a complex visual array. Neuropsychologia 17, 493–501 (1979).
Zihl, J. & von Cramon, D. The contribution of the 'second' visual system to directed visual attention in man. Brain 102, 835–856 (1979).
Benevento, L. A. & Port, J. D. Single neurons with both form/color differential responses and saccade-related responses in the nonretinotopic pulvinar of the behaving macaque monkey. Vis. Neurosci. 12, 523–544 (1995).
Petersen, S. E., Robinson, D. L. & Keys, W. Pulvinar nuclei of the behaving rhesus monkey: visual responses and their modulation. J. Neurophysiol. 54, 867–886 (1985).
Desimone, R., Wessinger, M., Thomas, L. & Schneider, W. Attentional control of visual perception: cortical and subcortical mechanisms. Cold Spring Harb. Symp. Quant. Biol. 55, 963–971 (1990).
Karnath, H. O., Himmelbach, M. & Rorden, C. The subcortical anatomy of human spatial neglect: putamen, caudate nucleus and pulvinar. Brain 125, 350–360 (2002).
Ward, R., Danziger, S., Owen, V. & Rafal, R. Deficits in spatial coding and feature binding following damage to spatiotopic maps in the human pulvinar. Nature Neurosci. 5, 99–100 (2002).
Wilke, M., Mueller, K. M. & Leopold, D. A. Neural activity in the visual thalamus reflects perceptual suppression. Proc. Natl Acad. Sci. USA 106, 9465–9470 (2009).
Padmala, S., Lim, S.-L. & Pessoa, L. Pulvinar and affective significance: responses track moment-to-moment visibility. Front. Hum. Neurosci. 4, 1–9 (2010).
Pessoa, L. & Ungerleider, L. G. Neural correlates of change detection and change blindness in a working memory task. Cereb. Cortex 14, 511–520 (2004).
Shipp, S. The functional logic of cortico-pulvinar connections. Phil. Trans. R. Soc. Lond. B 358, 1605–1624 (2003).
Lyon, D. C., Nassi, J. J. & Callaway, E. M. A disynaptic relay from superior colliculus to dorsal stream visual cortex in macaque monkey. Neuron 65, 270–279 (2010).
Berman, R. A. & Wurtz, R. H. Functional identification of a pulvinar path from superior colliculus to cortical area MT. J. Neurosci. 30, 6342–6354 (2010).
Shipp, S. The brain circuitry of attention. Trends Cogn. Sci. 8, 223–230 (2004).
Jones, E. G. & Burton, H. A projection from the medial pulvinar to the amygdala in primates. Brain Res. 104, 142–147 (1976).
Romanski, L. M., Giguere, M., Bates, J. F. & Goldman-Rakic, P. S. Topographic organization of medial pulvinar connections with the prefrontal cortex in the rhesus monkey. J. Comp. Neurol. 379, 313–332 (1997).
Aggleton, J. P., Burton, M. J. & Passingham, R. E. Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta). Brain Res. 190, 347–368 (1980).
Sherman, S. M. & Guillery, R. W. Exploring the Thalamus. (Academic Press, San Diego, 2001).
Cowey, A. The 30th Sir Frederick Bartlett lecture. Fact, artefact, and myth about blindsight. Q. J. Exp. Psychol. A 57, 577–609 (2004).
Chen, C. M. et al. Functional anatomy and interaction of fast and slow visual pathways in macaque monkeys. Cereb. Cortex 17, 1561–1569 (2007).
Nakamura, H., Gattass, R., Desimone, R. & Ungerleider, L. G. The modular organization of projections from areas V1 and V2 to areas V4 and TEO in macaques. J. Neurosci. 13, 3681–3691 (1993).
Felleman, D. J. & Van Essen, D. C. Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb. Cortex 1, 1–47 (1991).
Lamme, V. A. & Roelfsema, P. R. The distinct modes of vision offered by feedforward and recurrent processing. Trends Neurosci. 23, 571–579 (2000).
Yukie, M. & Iwai, E. Direct projection from the dorsal lateral geniculate nucleus to the prestriate cortex in macaque monkeys. J. Comp. Neurol. 201, 81–97 (1981).
Bullier, J. & Kennedy, H. Projection of the lateral geniculate nucleus onto cortical area V2 in the macaque monkey. Exp. Brain Res. 53, 168–172 (1983).
Schmid, M. C., Panagiotaropoulos, T., Augath, M. A., Logothetis, N. K. & Smirnakis, S. M. Visually driven activation in macaque areas V2 and V3 without input from the primary visual cortex. PLoS ONE 4, e5527 (2009).
Boyer, J. L., Harrison, S. & Ro, T. Unconscious processing of orientation and color without primary visual cortex. Proc. Natl Acad. Sci. USA 102, 16875–16879 (2005).
Schmid, M. C. et al. Blindsight depends on the lateral geniculate nucleus. Nature 466, 373–377 (2010).
Rempel-Clower, N. L. & Barbas, H. The laminar pattern of connections between prefrontal and anterior temporal cortices in the Rhesus monkey is related to cortical structure and function. Cereb. Cortex 10, 851–865 (2000).
Bar, M. A cortical mechanism for triggering top-down facilitation in visual object recognition. J. Cogn. Neurosci. 15, 600–609 (2003).
Bullier, J. Integrated model of visual processing. Brain Res. Brain Res. Rev. 36, 96–107 (2001).
Kveraga, K., Boshyan, J. & Bar, M. Magnocellular projections as the trigger of top–down facilitation in recognition. J. Neurosci. 27, 13232–13240 (2007).
Barrett, L. F. & Bar, M. See it with feeling: affective predictions during object perception. Phil. Trans. R. Soc. Lond. B 364, 1325–1334 (2009).
Capalbo, M., Postma, E. & Goebel, R. Combining structural connectivity and response latencies to model the structure of the visual system. PLoS Comput. Biol. 4, e1000159 (2008).
Nowak, L. G. & Bullier, J. in Cerebral Cortex: Extrastriate Cortex in Primate (eds Rockland, K., Kass, J. & Peters, A.) 205–241 (Plenum, New York, 1997).
Sugase, Y., Yamane, S., Ueno, S. & Kawano, K. Global and fine information coded by single neurons in the temporal visual cortex. Nature 400, 142–147 (1999).
Sripati, A. P. & Olson, C. R. Representing the forest before the trees: a global advantage effect in monkey inferotemporal cortex. J. Neurosci. 29, 7788–7796 (2009).
Rudrauf, D. et al. Rapid interactions between the ventral visual stream and emotion-related structures rely on a two-pathway architecture. J. Neurosci. 28, 2793–2803 (2008).
Andino, S. L., Menendez, R. G., Khateb, A., Landis, T. & Pegna, A. J. Electrophysiological correlates of affective blindsight. Neuroimage 44, 581–589 (2009).
Rotshtein, P. et al. Amygdala damage affects event-related potentials for fearful faces at specific time windows. Hum. Brain Mapp. 31, 1089–1105 (2010).
Ward, R., Calder, A. J., Parker, M. & Arend, I. Emotion recognition following human pulvinar damage. Neuropsychologia 45, 1973–1978 (2007).
Ward, R., Danziger, S. & Bamford, S. Response to visual threat following damage to the pulvinar. Curr. Biol. 15, 571–573 (2005).
Vuilleumier, P., Richardson, M. P., Armony, J. L., Driver, J. & Dolan, R. J. Distant influences of amygdala lesion on visual cortical activation during emotional face processing. Nature Neurosci. 7, 1271–1278 (2004).
Ghashghaei, H. T., Hilgetag, C. C. & Barbas, H. Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage 34, 905–923 (2007).
Averbeck, B. B. & Seo, M. The statistical neuroanatomy of frontal networks in the macaque. PLoS Comput. Biol. 4, e1000050 (2008).
Modha, D. S. & Singh, R. Network architecture of the long-distance pathways in the macaque brain. Proc. Natl Acad. Sci. USA 107, 13485–13490 (2010).
Lim, S. L., Padmala, S. & Pessoa, L. Segregating the significant from the mundane on a moment-to-moment basis via direct and indirect amygdala contributions. Proc. Natl Acad. Sci. USA 106, 16841–16846 (2009).
Whalen, P. J. Fear, vigilance, and ambiguity: initial neuroimaging studies of the human amygdala. Curr. Dir. Psychol.Sci. 7, 177–188 (1998).
Sander, D., Grafman, J. & Zalla, T. The human amygdala: an evolved system for relevance detection. Rev. Neurosci. 14, 303–316 (2003).
Hsu, M., Bhatt, M., Adolphs, R., Tranel, D. & Camerer, C. F. Neural systems responding to degrees of uncertainty in human decision-making. Science 310, 1680–1683 (2005).
Pessoa, L. Emotion and cognition and the amygdala: from “what is it?” to “what's to be done?” Neuropsychologia 48, 3416–3429 (2010).
Grossberg, S. & Levine, D. S. Neural dynamics of attentionally modulated Pavlovian conditioning: blocking, interstimulus interval, and secondary reinforcement. Appl. Opt. 26, 5015–5030 (1987).
Aggleton, J. P. (ed.) The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction (John Wiley & Sons, New York, 1992).
Aggleton, J. (ed.) The Amygdala: A Functional Analysis (Oxford Univ. Press, Oxford, 2000).
Ouellette, B. G. & Casanova, C. Overlapping visual response latency distributions in visual cortices and LP-pulvinar complex of the cat. Exp. Brain Res. 175, 332–341 (2006).
Schmolesky, M. T. et al. Signal timing across the macaque visual system. J. Neurophysiol. 79, 3272–3278 (1998).
Boehnke, S. E. & Munoz, D. P. On the importance of the transient visual response in the superior colliculus. Curr. Opin. Neurobiol. 18, 544–551 (2008).
Leonard, C. M., Rolls, E. T., Wilson, F. A. & Baylis, G. C. Neurons in the amygdala of the monkey with responses selective for faces. Behav. Brain Res. 15, 159–176 (1985).
Kuraoka, K. & Nakamura, K. Responses of single neurons in monkey amygdala to facial and vocal emotions. J. Neurophysiol. 97, 1379–1387 (2007).
Nakamura, K., Mikami, A. & Kubota, K. Activity of single neurons in the monkey amygdala during performance of a visual discrimination task. J. Neurophysiol. 67, 1447–1463 (1992).
Oya, H., Kawasaki, H., Howard, M. A. & Adolphs, R. Electrophysiological responses in the human amygdala discriminate emotion categories of complex visual stimuli. J. Neurosci. 22, 9502–9512 (2002).
Tovee, M. J. & Rolls, E. T. Information encoding in short firing rate epochs by single neurons in the primate temporal visual cortex. Vis. Cogn. 2, 35–58 (1995).
Yoshor, D., Bosking, W. H., Ghose, G. M. & Maunsell, J. H. Receptive fields in human visual cortex mapped with surface electrodes. Cereb. Cortex 17, 2293–2302 (2007).
King, A. J. & Nelken, I. Unraveling the principles of auditory cortical processing: can we learn from the visual system? Nature Neurosci. 12, 698–701 (2009).
Acknowledgements
The authors thank A. Anticevic, L. Oliveira, M. Pereira, R. Todd, and S. Wang for feedback on the manuscript. They also thank L. Barrett and two anonymous reviewers for comments. The authors' research is supported by grants from the National Institute of Mental Health (R01 MH071589 to L.P. and R01 MH080721 to R.A.), the National Institute of Neurological Disorders and Stroke (P01 NS019632 to R.A.), the Simons Foundation Autism Research Initiative and the National Science Foundation (NSF 0926,544).
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Glossary
- Attentional blink
-
A phenomenon that occurs in experiments in which a rapid stream of visual items is presented to an observer whose task is to detect two targets within the stream. When the two targets are separated in time by a brief interval (for example, 200–500ms), the successful detection of the first target impairs detection of the second one (as if the participant blinked) owing to limited processing capacity.
- Backward masking
-
A phenomenon that occurs in experimental paradigms in which a target visual stimulus is followed by another salient visual stimulus that 'masks' the perception of the target stimulus, making its detection or recognition difficult or impossible. Visual masking is commonly used to manipulate visual awareness.
- Blindsight
-
The ability, in humans or monkeys, to respond to visual stimuli without consciously perceiving them — a situation that may ensue following a lesion to the primary visual cortex.
- Continuous flash suppression
-
A technique in which a fixed image shown to one eye is suppressed by a stream of rapidly changing images flashed to the other eye. The technique is used to manipulate visual awareness.
- Labelled line
-
A processing architecture in which a separate pathway conveys information that is specific to a class of sensory stimuli owing to, for example, receptor specificity (for example, pain and touch conveyed by particular somatosensory channels).
- Magnocellular system
-
A visual pathway from the retina to the cortex that conveys relatively fast, transient and wavelength-insensitive information.
- Path analysis
-
A statistical method to investigate the relationship between multiple variables.
- Source modelling
-
A set of techniques that attempt to estimate the neural 'sources' of the electrical or magnetic signals that are measured at external sensors (for example, at the scalp in the case of electroencephalography).
- Visual search
-
An experimental paradigm in which subjects are asked to indicate the presence or absence of a 'target' item (for example, a fearful face) among an array of distractor items (for example, neutral faces).
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Pessoa, L., Adolphs, R. Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance. Nat Rev Neurosci 11, 773–782 (2010). https://doi.org/10.1038/nrn2920
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DOI: https://doi.org/10.1038/nrn2920
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