Hysteresis tích cực trong nhận diện cảm xúc: Các vùng thị giác xử lý khuôn mặt liên quan đến sự bền vững cảm nhận, điều hòa các tương tác giữa vùng đảo trước và vỏ não trước trán giữa

Springer Science and Business Media LLC - Tập 22 - Trang 1275-1289 - 2022
Andreia Verdade1,2, Teresa Sousa1,2, João Castelhano1,2, Miguel Castelo-Branco1,2,3
1Coimbra Institute for Biomedical Imaging and Translational Research (CIBIT), University of Coimbra, Coimbra, Portugal
2Institute of Nuclear Sciences Applied to Health (ICNAS), University of Coimbra, Coimbra, Portugal
3Faculty of Medicine, University of Coimbra, Coimbra, Portugal

Tóm tắt

Nhận diện cảm xúc khuôn mặt có thể được nghiên cứu từ góc độ của các hệ thống động mà đầu ra của chúng có thể phụ thuộc không chỉ vào đầu vào hiện tại mà còn vào lịch sử trước đó — một hiện tượng được gọi là hiện tượng tắc nghẽn. Trong lĩnh vực thần kinh nhận thức, hiện tượng tắc nghẽn đã được mô tả như là tích cực (sự bền vững cảm nhận) hoặc tiêu cực (mệt mỏi cảm nhận hiện tại) tùy thuộc vào việc chuyển giao cảm nhận xảy ra muộn hơn hay sớm hơn so với sự thay đổi kích thích vật lý thực sự. Tuy nhiên, các tương quan thần kinh của hiện tượng này vẫn chưa được xác định rõ ràng. Chúng tôi đã sử dụng các chuyển tiếp động giữa các biểu hiện cảm xúc và kết hợp đánh giá hành vi với hình ảnh cộng hưởng từ chức năng (fMRI) để điều tra hệ thống thần kinh cơ bản của hiện tượng tắc nghẽn cảm nhận trong nhận diện cảm xúc khuôn mặt. Các phát hiện của chúng tôi chỉ ra sự tham gia của các vùng thị giác chọn lọc khuôn mặt — khu vực khuôn mặt fusiform (FFA) và rãnh thượng thời gian (STS) — trong sự bền vững cảm nhận cũng như sự tham gia của đảo trước bên phải. Hơn nữa, phân tích kết nối chức năng đã tiết lộ một sự tương tác giữa đảo trước bên phải và vỏ não trước trán giữa, mà cho thấy phụ thuộc vào sự hiện diện của hiện tượng tắc nghẽn tích cực. Kết quả của chúng tôi hỗ trợ giả thuyết rằng các vùng cao hơn có liên quan đến sự ổn định cảm nhận và quyết định trong suốt sự bền vững cảm nhận (hiện tượng tắc nghẽn tích cực) và đóng góp bằng chứng về vai trò của đảo trước như một trung tâm thông tin cảm giác trong quyết định cảm nhận.

Từ khóa

#hysteresis #nhận diện cảm xúc #hình ảnh cộng hưởng từ chức năng #vùng thị giác #ổn định cảm nhận #đảo trước #vỏ não trước trán giữa

Tài liệu tham khảo

Alexander, W. H., & Brown, J. W. (2011). Medial prefrontal cortex as an action-outcome predictor. Nature Neuroscience, 14, 1338–1344. https://doi.org/10.1038/nn.2921 Barbalat, G., Rouault, M., Bazargani, N., Shergill, S., & Blakemore, S. J. (2012). The influence of prior expectations on facial expression discrimination in schizophrenia. Psychological Medicine, 42(11), 2301–2311. https://doi.org/10.1017/S0033291712000384 Behrmann, M., Thomas, C., & Humphreys, K. (2006). Seeing it differently: Visual processing in autism. Trends in Cognitive Sciences, 10(6), 258–264. https://doi.org/10.1016/j.tics.2006.05.001 Beissner, F., Meissner, K., Bär, K. J., & Napadow, V. (2013). The autonomic brain: An activation likelihood estimation meta-analysis for central processing of autonomic function. The Journal of Neuroscience, 33(25), 10503–10511. https://doi.org/10.1523/JNEUROSCI.1103-13.2013 Bernstein, M., Erez, Y., Blank, I., & Yovel, G. (2018). An Integrated Neural Framework for Dynamic and Static Face Processing. Scientific Reports, 8(1), 7036. https://doi.org/10.1038/s41598-018-25405-9 Billeke, P., Ossandon, T., Perrone-Bertolotti, M., Kahane, P., Bastin, J., Jerbi, K., Lachaux, J. P., & Fuentealba, P. (2020). Human Anterior Insula Encodes Performance Feedback and Relays Prediction Error to the Medial Prefrontal Cortex. Cerebral Cortex, 30(7), 4011–4025. https://doi.org/10.1093/cercor/bhaa017 Blake, R., Sobel, K. V., & Gilroy, L. A. (2003). Visual motion retards alternations between conflicting perceptual interpretations. Neuron, 39(5), 869–878. https://doi.org/10.1016/S0896-6273(03)00495-1 Castelhano, J., Duarte, I. C., Wibral, M., Rodriguez, E., & Castelo-Branco, M. (2014). The dual facet of gamma oscillations: separate visual and decision making circuits as revealed by simultaneous EEG/fMRI. Human Brain Mapping, 35(10), 5219–35. https://doi.org/10.1002/hbm.22545 Castelhano, J., Duarte, I. C., Abuhaiba, S. I., Rito, M., Sales, F., & Castelo-Branco, M. (2017). Cortical functional topography of high-frequency gamma activity relates to perceptual decision: An intracranial study. PLoS One, 12(10), 1–15. https://doi.org/10.1371/journal.pone.0186428 Chand, G. B., & Dhamala, M. (2016). The salience network dynamics in perceptual decision-making. Neuroimage, 134, 85–93. https://doi.org/10.1016/j.neuroimage.2016.04.018 Chang, L. J., Yarkoni, T., Khaw, M. W., & Sanfey, A. G. (2013). Decoding the role of the insula in human cognition: Functional parcellation and large-scale reverse inference. Cerebral Cortex, 23(3), 739–749. https://doi.org/10.1093/cercor/bhs065 Chen, X., & He, S. (2004). Local factors determine the stabilization of monocular ambiguous and binocular rivalry stimuli. Current Biology, 14(11), 1013–1017. https://doi.org/10.1016/j.cub.2004.05.042 Craig, A. D. (2009). How do you feel - now? The anterior insula and human awareness. Nature Reviews. Neuroscience, 10(1), 59–70. https://doi.org/10.1038/nrn2555 De Winter, F. L., Zhu, Q., Van den Stock, J., Nelissen, K., Peeters, R., de Gelder, B., Vanduffel, W., & Vandenbulcke, M. (2015). Lateralization for dynamic facial expressions in human superior temporal sulcus. Neuroimage, 1, 340–352. https://doi.org/10.1016/j.neuroimage.2014.11.020 Direito, B., Lima, J., Simões, M., Sayal, A., Sousa, T., Lührs, M., et al. (2019). Targeting dynamic facial processing mechanisms in superior temporal sulcus using a novel fMRI neurofeedback target. Neuroscience, 406, 97–108. https://doi.org/10.1016/j.neuroscience.2019.02.024 Dubé, S. P. (1997). Visual bases for the perception of facial expressions: A look at some dynamic aspects. Concordia University. Duchaine, B., & Yovel, G. (2015). A revised neural framework for face processing. Annual Review of Vision Science, 1, 393–416. https://doi.org/10.1146/annurev-vision-082114-035518 Ebisch, S. J. H., Mantini, D., Romanelli, R., Tommasi, M., Perrucci, M. G., Romani, G. L., Colom, R., & Saggino, A. (2013). Long-range functional interactions of anterior insula and medial frontal cortex are differently modulated by visuospatial and inductive reasoning tasks. Neuroimage, 78, 426–438. https://doi.org/10.1016/j.neuroimage.2013.04.058 Eckert, M. A., Menon, V., Walczak, A., Ahlstrom, J., Denslow, S., Horwitz, A., & Dubno, J. R. (2009). At the heart of the ventral attention system: The right anterior insula. Human Brain Mapping, 30(8), 2530–2541. https://doi.org/10.1002/hbm.20688 Ekman, P., & Friesen, W. V. (1978). Facial Action Coding System: A Technique for the Measurement of Facial Movement. Consulting Psychologists Press. Euston, D. R., Gruber, A. J., & McNaughton, B. L. (2012). The Role of Medial Prefrontal Cortex in Memory and Decision Making. Neuron, 76(6), 1057–1070. https://doi.org/10.1016/j.neuron.2012.12.002 Fan, X., Wang, F., Shao, H., Zhang, P., & He, S. (2020). The bottom-up and top-down processing of faces in the human occipitotemporal cortex. Elife, 9, e48764. https://doi.org/10.7554/eLife.48764 Fletcher, P. C., & Frith, C. D. (2009). Perceiving is believing: A Bayesian approach to explaining the positive symptoms of schizophrenia. Nature Reviews. Neuroscience, 10, 48–58. https://doi.org/10.1038/nrn2536 Fonov, V., Evans, A. C., Botteron, K., Almli, C. R., McKinstry, R. C., & Collins, D. L. (2011). Unbiased average age-appropriate atlases for pediatric studies. Neuroimage, 54(1), 313–327. https://doi.org/10.1016/j.neuroimage.2010.07.033 Friston, K. J., Buechel, C., Fink, G. R., Morris, J., Rolls, E., & Dolan, R. J. (1997). Psychophysiological and modulatory interactions in neuroimaging. Neuroimage, 6(3), 218–229. https://doi.org/10.1006/nimg.1997.0291 Fritsche, M., Mostert, P., & de Lange, F. P. (2017). Opposite effects of recent history on perception and decision. Current Biology. https://doi.org/10.1016/j.cub.2017.01.006 Gazzaley, A., Rissman, J., & D’Esposito, M. (2004). Functional connectivity during working memory maintenance. Cognitive, Affective, & Behavioral Neuroscience, 4(4), 580–599. https://doi.org/10.3758/cabn.4.4.580 Gepshtein, S., & Kubovy, M. (2005). Stability and change in perception: Spatial organization in temporal context. Experimental Brain Research, 160(4), 487–495. https://doi.org/10.1007/s00221-004-2038-3 Gu, X., Hof, P. R., Friston, K. J., & Fan, J. (2013). Anterior insular cortex and emotional awareness. The Journal of Comparative Neurology, 521(15), 3371–3388. https://doi.org/10.1002/cne.23368 Hadad, B. S., & Schwartz, S. (2019). Perception in autism does not adhere to weber’s law. Elife, 8, e42223. https://doi.org/10.7554/eLife.42223 Hock, H. S., & Schöner, G. (2011). Measuring perceptual hysteresis with the modified method of limits: Dynamics at the threshold. In Solomon, J. A. (Ed.), Fechner’s legacy in psychology: 150 years of elementary psychophysics (pp. 63–85). BRILL. Hsu, S. M., & Wu, Z. R. (2019). The roles of preceding stimuli and preceding responses on assimilative and contrastive sequential effects during facial expression perception. Cognition & Emotion, 34(5), 890–905. https://doi.org/10.1080/02699931.2019.1696752 Jiles, D. C., & Atherton, D. L. (1986). Theory of ferromagnetic hysteresis. Journal of Magnetism and Magnetic Materials. https://doi.org/10.1016/0304-8853(86)90066-1 Kamachi, M., Bruce, V., Mukaida, S., Gyoba, J., Yoshikawa, S., & Akamatsu, S. (2013). Dynamic properties influence the perception of facial expressions. Perception, 42(11), 1266–1278. https://doi.org/10.1068/p3131n Kanwisher, N., McDermott, J., & Chun, M. M. (1997). The fusiform face area: A module in human extrastriate cortex specialized for face perception. The Journal of Neuroscience, 17(11), 4302–4311. https://doi.org/10.1523/jneurosci.17-11-04302.1997 Karolis, V. R., Corbetta, M., & Thiebaut de Schotten, M. (2019). The architecture of functional lateralisation and its relationship to callosal connectivity in the human brain. Nature Communications, 10(1417). https://doi.org/10.1038/s41467-019-09344-1 Kersten, D., & Yuille, A. (2003). Bayesian models of object perception. Current Opinion in Neurobiology, 13(2), 150–158. https://doi.org/10.1016/S0959-4388(03)00042-4 Kleinschmidt, A., Büchel, C., Hutton, C., Friston, K. J., & Frackowiak, R. S. J. (2002). The neural structures expressing perceptual hysteresis in visual letter recognition. Neuron, 34(4), 659–666. https://doi.org/10.1016/S0896-6273(02)00694-3 Kobayashi H, Hara F. (1993). Dynamic recognition of basic facial expressions by discrete-time recurrent neural network. In: Proceedings of 1993 International Conference on Neural Networks (IJCNN-93-Nagoya, Japan). Nagoya, Japan. p. 155–158. LaBar, K. S., Crupain, M. J., Voyvodic, J. T., & McCarthy, G. (2003). Dynamic perception of facial affect and identity in the human brain. Cerebral Cortex, 13(10), 1023–1033. https://doi.org/10.1093/cercor/13.10.1023 Lamichhane, B., Adhikari, B. M., & Dhamala, M. (2016). The activity in the anterior insulae is modulated by perceptual decision-making difficulty. Neuroscience. https://doi.org/10.1016/j.neuroscience.2016.04.016 Liaci, E., Fischer, A., Atmanspacher, H., Heinrichs, M., Van Elst, L. T., & Kornmeier, J. (2018). Positive and negative hysteresis effects for the perception of geometric and emotional ambiguities. PLoS One, 13(9), e020. Liberman, A., Manassi, M., & Whitney, D. (2018). Serial dependence promotes the stability of perceived emotional expression depending on face similarity. Attention, Perception, & Psychophysics, 80(6), 1461–1473. https://doi.org/10.3758/s13414-018-1533-8 Lopresti-Goodman, S. M., Turvey, M. T., & Frank, T. D. (2013). Negative hysteresis in the behavioral dynamics of the affordance “graspable”. Attention, Perception, & Psychophysics. https://doi.org/10.3758/s13414-013-0437-x Lucey P, Cohn JF, Kanade T, Saragih J, Ambadar Z, Matthews I. (2010). The extended Cohn-Kanade dataset (CK+): A complete dataset for action unit and emotion-specified expression. In: 2010 IEEE Computer Society Conference on Computer Vision and Pattern Recognition - Workshops, CVPRW 2010. San Francisco, CA. p. 94–101. Luenberger, D. G. (1979). Introduction to Dynamic Systems Theory, Models, and Applications. John Wiley & Sons. Martin, J. R., Dezecache, G., Pressnitzer, D., Nuss, P., Dokic, J. Ô., Bruno, N., Pacherie, E., & Franck, N. (2014). Perceptual hysteresis as a marker of perceptual inflexibility in schizophrenia. Consciousness and Cognition, 30, 62–72. https://doi.org/10.1016/j.concog.2014.07.014 McLaren, D. G., Ries, M. L., Xu, G., & Johnson, S. C. (2012). A generalized form of context-dependent psychophysiological interactions (gPPI): A comparison to standard approaches. Neuroimage, 61(4), 1277–1286. https://doi.org/10.1016/j.neuroimage.2012.03.068 Mei, G., Chen, S., & Dong, B. (2019). Working memory maintenance modulates serial dependence effects of perceived emotional expression. Frontiers in Psychology, 10, 1610. https://doi.org/10.3389/fpsyg.2019.01610 Menon, V. (2015). Salience Network. In Brain Mapping: An Encyclopedic Reference (pp. 597–611). Academic Press: Elsevier. Menon, V., & Uddin, L. (2010). Saliency, switching, attention and control: A network model of insula function. Brain Structure & Function, 214(5–6), 655–667. https://doi.org/10.1007/s00429-010-0262-0 Nakamura, A., Maess, B., Knösche, T. R., & Friederici, A. D. (2014). Different hemispheric roles in recognition of happy expressions. PLoS One, 9(2), e88628. https://doi.org/10.1371/journal.pone.0088628 Orbach, J., Ehrlich, D., & Heath, H. A. (1963). Reversibility of the Necker Cube. I. An examination of the concept of “satiation of orientation”. Perceptual and Motor Skills, 17, 439–458. https://doi.org/10.2466/pms.1963.17.2.439 Pearson, J., & Brascamp, J. (2008). Sensory memory for ambiguous vision. Trends in Cognitive Sciences, 12(9), 334–341. https://doi.org/10.1016/j.tics.2008.05.006 Pessoa, L., & Padmala, S. (2005). Quantitative prediction of perceptual decisions during near-threshold fear detection. Proceedings of the National Academy of Sciences of the United States of America, 102(15), 5612–5617. https://doi.org/10.1073/pnas.0500566102 Pisarchik, A. N., Jaimes-Reátegui, R., Magallón-García, C. D. A., & Castillo-Morales, C. O. (2014). Critical slowing down and noise-induced intermittency in bistable perception: Bifurcation analysis. Biological Cybernetics, 108(4), 397–404. https://doi.org/10.1007/s00422-014-0607-5 Russell, J. A. (1980). A circumplex model of affect. Journal of Personality and Social Psychology, 39(6), 1161–1178. https://doi.org/10.1037/h0077714 Sacharin, V., Sander, D., & Scherer, K. R. (2012). The perception of changing emotion expressions. Cognition & Emotion. https://doi.org/10.1080/02699931.2012.656583 Said, C. P., Haxby, J. V., & Todorov, A. (2011). Brain systems for assessing the affective value of faces. Philosophical Transactions of the Royal Society B: Biological Sciences, 366(1571), 1660–1670. https://doi.org/10.1098/rstb.2010.0351 Sato, W., Kochiyama, T., Yoshikawa, S., Naito, E., & Matsumura, M. (2004). Enhanced neural activity in response to dynamic facial expressions of emotion: An fMRI study. Cognitive Brain Research, 20(1), 81–91. https://doi.org/10.1016/j.cogbrainres.2004.01.008 Sato, W., Kochiyama, T., Uono, S., & Yoshikawa, S. (2010). Amygdala integrates emotional expression and gaze direction in response to dynamic facial expressions. Neuroimage, 50(4), 1658–1665. https://doi.org/10.1016/j.neuroimage.2010.01.049 Sayal, A., Sousa, T., Duarte, J. V., Costa, G. N., Martins, R., & Castelo-Branco, M. (2020). Identification of competing neural mechanisms underlying positive and negative perceptual hysteresis in the human visual system. Neuroimage, 221(July). https://doi.org/10.1016/j.neuroimage.2020.117153 Schwiedrzik, C. M., Ruff, C. C., Lazar, A., Leitner, F. C., Singer, W., & Melloni, L. (2014). Untangling perceptual memory: Hysteresis and adaptation map into separate cortical networks. Cerebral Cortex, 24(5), 1152–1164. https://doi.org/10.1093/cercor/bhs396 Schwiedrzik, C. M., Sudmann, S. S., Thesen, T., Wang, X., Groppe, D., Mégevand, P., Doyle, W., Mehta, A. D., Devinsky, O., & Melloni L. (2018). Medial prefrontal cortex supports perceptual memory. Current Biology, 28(18), PR1094-PR1095. Seeley, W. W. (2019). The salience network: A neural system for perceiving and responding to homeostatic demands. The Journal of Neuroscience, 39(50), 9878–9882. https://doi.org/10.1523/JNEUROSCI.1138-17.2019 Singer, T., Critchley, H. D., & Preuschoff, K. (2009). A common role of insula in feelings, empathy and uncertainty. Trends in Cognitive Sciences, 13(8), 334–340. https://doi.org/10.1016/j.tics.2009.05.001 Stoner, E. C., & Wohlfarth, E. P. (1991). A mechanism of magnetic hysteresis in heterogeneous alloys. IEEE Transactions on Magnetics, 27(4), 3475–3518. https://doi.org/10.1109/TMAG.1991.1183750 Thielscher, A., & Pessoa, L. (2007). Neural correlates of perceptual choice and decision making during fear-disgust discrimination. The Journal of Neuroscience, 27(11), 2908–2917. https://doi.org/10.1523/JNEUROSCI.3024-06.2007 Touroutoglou, A., Hollenbeck, M., Dickerson, B. C., & Feldman, B. L. (2012). Dissociable large-scale networks anchored in the right anterior insula subserve affective experience and attention. Neuroimage, 60(4), 1947–1958. https://doi.org/10.1016/j.neuroimage.2012.02.012 Trautmann, S. A., Fehr, T., & Herrmann, M. (2009). Emotions in motion: Dynamic compared to static facial expressions of disgust and happiness reveal more widespread emotion-specific activations. Brain Research, 1284, 100–115. https://doi.org/10.1016/j.brainres.2009.05.075 Trautmann-Lengsfeld, S. A., Domínguez-Borràs, J., Escera, C., Herrmann, M., & Fehr, T. (2013). The Perception of Dynamic and Static Facial Expressions of Happiness and Disgust Investigated by ERPs and fMRI Constrained Source Analysis. PLoS One, 8(6), e66997. https://doi.org/10.1371/journal.pone.0066997 Uddin, L. Q., Nomi, J. S., Hébert-Seropian, B., Ghaziri, J., & Boucher, O. (2017). Structure and Function of the Human Insula. Journal of Clinical Neurophysiology, 34(4), 300–306. https://doi.org/10.1097/WNP.0000000000000377 Verdade, A., Castelhano, J., Sousa, T., & Castelo-Branco, M. (2020). How positive emotional content overrules perceptual history effects: Hysteresis in emotion recognition. Journal of Vision, 20(8), 1–15. https://doi.org/10.1167/JOV.20.8.19 Wang, Y., Metoki, A., Smith, D. V., Medaglia, J. D., Zang, Y., Benear, S., Popal, H., Lin, Y., & Olson, I. R. (2020). Multimodal mapping of the face connectome. Nature Human Behaviour, 4, 397–411. https://doi.org/10.1038/s41562-019-0811-3 Warburg, E. (1881). Magnetische untersuchungen [Magnetic investigations]. Annalen der Physik, 249(5), 141–164. Webster, M. A., Kaping, D., Mizukami, Y., & Duhamel, P. (2004). Adaptation to natural facial categories. Nature, 428(6982), 557–561. https://doi.org/10.1038/nature02420 Wicker, B., Keysers, C., Plailly, J., Royet, J. P., Gallese, V., & Rizzolatti, G. (2003). Both of us disgusted in My insula: The common neural basis of seeing and feeling disgust. Neuron, 40(3), 655–664. https://doi.org/10.1016/S0896-6273(03)00679-2 Williams, D., Phillips, G., & Sekuler, R. (1986). Hysteresis in the perception of motion direction as evidence for neural cooperativity. Nature, 324(6094), 253–255. https://doi.org/10.1038/324253a0 Witthoft, N., Sha, L., Winawer, J., & Kiani, R. (2018). Sensory and decision-making processes underlying perceptual adaptation. Journal of Vision, 18(8), 10. https://doi.org/10.1167/18.8.10 Xue, G., Lu, Z., Levin, I. P., & Bechara, A. (2010). The impact of prior risk experiences on subsequent risky decision-making: The role of the insula. Neuroimage, 50(2), 709–716. https://doi.org/10.1016/j.neuroimage.2009.12.097 Zhang, Y., Zhou, W., Wang, S., Zhou, Q., Wang, H., Zhang, B., Huang, J., Hong, B., & Wang, X. (2018). The roles of subdivisions of human insula in emotion perception and auditory processing. Cerebral Cortex, 29(2), 1–12.