Ultra High Field fMRI of Human Superior Colliculi Activity during Affective Visual Processing.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
28 Jan 2020
28 Jan 2020
Historique:
received:
14
01
2019
accepted:
31
12
2019
entrez:
30
1
2020
pubmed:
30
1
2020
medline:
11
6
2020
Statut:
epublish
Résumé
Research on rodents and non-human primates has established the involvement of the superior colliculus in defensive behaviours and visual threat detection. The superior colliculus has been well-studied in humans for its functional roles in saccade and visual processing, but less is known about its involvement in affect. In standard functional MRI studies of the human superior colliculus, it is challenging to discern activity in the superior colliculus from activity in surrounding nuclei such as the periaqueductal gray due to technological and methodological limitations. Employing high-field strength (7 Tesla) fMRI techniques, this study imaged the superior colliculus at high (0.75 mm isotropic) resolution, which enabled isolation of the superior colliculus from other brainstem nuclei. Superior colliculus activation during emotionally aversive image viewing blocks was greater than that during neutral image viewing blocks. These findings suggest that the superior colliculus may play a role in shaping subjective emotional experiences in addition to its visuomotor functions, bridging the gap between affective research on humans and non-human animals.
Identifiants
pubmed: 31992744
doi: 10.1038/s41598-020-57653-z
pii: 10.1038/s41598-020-57653-z
pmc: PMC6987103
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1331Subventions
Organisme : NIBIB NIH HHS
ID : K01 EB019474
Pays : United States
Organisme : NIDCD NIH HHS
ID : R21 DC015888
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA193632
Pays : United States
Organisme : Generalitat de Catalunya (Government of Catalonia)
ID : 2017 SGR 01612
Références
Savjani, R. R., Katyal, S., Halfen, E., Kim, J. H. & Ress, D. Polar-angle representation of saccadic eye movements in human superior colliculus. NeuroImage 171, 199–208, https://doi.org/10.1016/J.NEUROIMAGE.2017.12.080 (2018).
doi: 10.1016/J.NEUROIMAGE.2017.12.080
pubmed: 29292132
DuBois, R. M. & Cohen, M. S. Spatiotopic organization in human superior colliculus observed with fMRI. NeuroImage 12, 63–70, https://doi.org/10.1006/NIMG.2000.0590 (2000).
doi: 10.1006/NIMG.2000.0590
pubmed: 10875903
White, B. J. et al. Superior colliculus neurons encode a visual saliency map during free viewing of natural dynamic video. Nature Communications 8, 14263, https://doi.org/10.1038/ncomms14263 (2017).
doi: 10.1038/ncomms14263
pubmed: 28117340
pmcid: 5286207
Gandhi, N. J. & Katnani, H. A. Motor Functions of the Superior Colliculus. Annual Review of Neuroscience 34, 205–231, https://doi.org/10.1146/annurev-neuro-061010-113728 (2011).
doi: 10.1146/annurev-neuro-061010-113728
pubmed: 21456962
pmcid: 3641825
Goldberg, M. E. & Wurtz, R. H. Activity of superior colliculus in behaving monkey. Journal of Neurophysiology 35, 560–574, https://doi.org/10.1152/jn.1972.35.4.560 (1972).
doi: 10.1152/jn.1972.35.4.560
pubmed: 4624740
Müller, J. R., Philiastides, M. G. & Newsome, W. T. Microstimulation of the superior colliculus focuses attention without moving the eyes. Proceedings of the National Academy of Sciences 102, 524–529, https://doi.org/10.1073/pnas.0408311101 (2005).
doi: 10.1073/pnas.0408311101
Ignashchenkova, A., Dicke, P. W., Haarmeier, T. & Thier, P. Neuron-specific contribution of the superior colliculus to overt and covert shifts of attention. Nature Neuroscience 7, 56–64, https://doi.org/10.1038/nn1169 (2004).
doi: 10.1038/nn1169
pubmed: 14699418
May, P. J. The mammalian superior colliculus: laminar structure and connections. Progress in Brain Research 151, 321–378, https://doi.org/10.1016/S0079-6123(05)51011-2 (2006).
doi: 10.1016/S0079-6123(05)51011-2
pubmed: 16221594
Edwards, S. B., Ginsburgh, C. L., Henkel, C. K. & Stein, B. E. Sources of subcortical projections to the superior colliculus in the cat. J. Comp. Neur. 309–330 (1979).
Basso, M. A. & May, P. J. Circuits for action and cognition: A View from the superior colliculus. Annual Review of Vision Science 3, 197–226, https://doi.org/10.1146/annurev-vision-102016-061234 (2017).
doi: 10.1146/annurev-vision-102016-061234
pubmed: 28617660
pmcid: 5752317
Tardif, E., Delacuisine, B., Probst, A. & Clarke, S. Intrinsic connectivity of human superior colliculus. Experimental Brain Research 166, 316–324, https://doi.org/10.1007/s00221-005-2373-z (2005).
doi: 10.1007/s00221-005-2373-z
pubmed: 16032404
da Silva, J. A. et al. Dissociation between the panicolytic effect of cannabidiol microinjected into the substantia nigra, pars reticulata, and fear-induced antinociception elicited by bicuculline administration in deep layers of the superior colliculus: The role of CB1-cannabi. European Journal of Pharmacology 758, 153–163, https://doi.org/10.1016/J.EJPHAR.2015.03.051 (2015).
doi: 10.1016/J.EJPHAR.2015.03.051
pubmed: 25841876
Almada, R. C. et al. Stimulation of the nigrotectal pathway at the level of the superior colliculus reduces threat recognition and causes a shift From avoidance to approach behavior. Frontiers in Neural Circuits 12, 36, https://doi.org/10.3389/fncir.2018.00036 (2018).
doi: 10.3389/fncir.2018.00036
pubmed: 29867370
pmcid: 5949341
Li, L. et al. Stress accelerates defensive responses to looming in mice and involves a locus coeruleus-superior colliculus projection. Current Biology 28, 859–871, https://doi.org/10.1016/J.CUB.2018.02.005 (2018).
doi: 10.1016/J.CUB.2018.02.005
pubmed: 29502952
Comoli, E. et al. Segregated anatomical input to sub-regions of the rodent superior colliculus associated with approach and defense. Frontiers in Neuroanatomy 6, 9, https://doi.org/10.3389/fnana.2012.00009 (2012).
doi: 10.3389/fnana.2012.00009
pubmed: 22514521
pmcid: 3324116
Bittencourt, A. S., Nakamura-Palacios, E. M., Mauad, H., Tufik, S. & Schenberg, L. C. Organization of electrically and chemically evoked defensive behaviors within the deeper collicular layers as compared to the periaqueductal gray matter of the rat. Neuroscience 133, 873–92, https://doi.org/10.1016/j.neuroscience.2005.03.012 (2005).
doi: 10.1016/j.neuroscience.2005.03.012
pubmed: 15916856
de Almeida, L. P. et al. Prior electrical stimulation of dorsal periaqueductal grey matter or deep layers of the superior colliculus sensitizes rats to anxiety-like behaviors in the elevated T-maze test. Behavioural Brain Research 170, 175–81, https://doi.org/10.1016/j.bbr.2006.02.020 (2006).
doi: 10.1016/j.bbr.2006.02.020
pubmed: 16569447
Forcelli, P. A. et al. Amygdala selectively modulates defensive responses evoked from the superior colliculus in non-human primates. Social Cognitive and Affective Neuroscience 11, 2009–2019, https://doi.org/10.1093/scan/nsw111 (2016).
doi: 10.1093/scan/nsw111
pubmed: 27510499
pmcid: 5141962
DesJardin, J. T. et al. Defense-like behaviors evoked by pharmacological disinhibition of the superior colliculus in the primate. Journal of Neuroscience 33, 150–5, https://doi.org/10.1523/JNEUROSCI.2924-12.2013 (2013).
doi: 10.1523/JNEUROSCI.2924-12.2013
pubmed: 23283329
Soares, S. C., Maior, R. S., Isbell, L. A., Tomaz, C. & Nishijo, H. Fast detector/first responder: interactions between the superior colliculus-pulvinar pathway and stimuli relevant to primates. Frontiers in Neuroscience 11, 67, https://doi.org/10.3389/fnins.2017.00067 (2017).
doi: 10.3389/fnins.2017.00067
pubmed: 28261046
pmcid: 5314318
Adolphs, R. Neural systems for recognizing emotion. Current Opinion in Neurobiology 12, 169–77, https://doi.org/10.1016/S0959-4388(02)00301-X (2002).
doi: 10.1016/S0959-4388(02)00301-X
pubmed: 12015233
McFadyen, J., Mattingley, J. B. & Garrido, M. I. An afferent white matter pathway from the pulvinar to the amygdala facilitates fear recognition. eLife 8, e40766, https://doi.org/10.7554/eLife.40766 (2019).
doi: 10.7554/eLife.40766
pubmed: 30648533
pmcid: 6335057
Celeghin, A., de Gelder, B. & Tamietto, M. From affective blindsight to emotional consciousness. Consciousness and Cognition 36, 414–425, https://doi.org/10.1016/J.CONCOG.2015.05.007 (2015).
doi: 10.1016/J.CONCOG.2015.05.007
pubmed: 26058355
Maior, R. S. et al. Superior colliculus lesions impair threat responsiveness in infant capuchin monkeys. Neuroscience Letters 504, 257–260, https://doi.org/10.1016/j.neulet.2011.09.042 (2011).
doi: 10.1016/j.neulet.2011.09.042
pubmed: 21970966
Almeida, I., Soares, S. C. & Castelo-Branco, M. The Distinct Role of the Amygdala, Superior Colliculus and Pulvinar in Processing of Central and Peripheral Snakes. PLoS One 10, e0129949, https://doi.org/10.1371/journal.pone.0129949 (2015).
doi: 10.1371/journal.pone.0129949
pubmed: 26075614
pmcid: 4467980
Tamietto, M., Pullens, P., De Gelder, B., Weiskrantz, L. & Goebel, R. Subcortical connections to human amygdala and changes following destruction of the visual cortex. Current Biology 22, 1449–1455, https://doi.org/10.1016/j.cub.2012.06.006 (2012).
doi: 10.1016/j.cub.2012.06.006
pubmed: 22748315
Rafal, R. D. et al. Connectivity between the superior colliculus and the amygdala in humans and macaque monkeys: virtual dissection with probabilistic DTI tractography. Journal of Neurophysiology 114, 1947–1962, https://doi.org/10.1152/jn.01016.2014 (2015).
doi: 10.1152/jn.01016.2014
pubmed: 26224780
pmcid: 4579293
Koller, K., Rafal, R. D., Platt, A. & Mitchell, N. D. Orienting toward threat: Contributions of a subcortical pathway transmitting retinal afferents to the amygdala via the superior colliculus and pulvinar. Neuropsychologia pii: S0028, 30027–7, https://doi.org/10.1016/J.NEUROPSYCHOLOGIA.2018.01.027 (2018).
doi: 10.1016/J.NEUROPSYCHOLOGIA.2018.01.027
Fries, W. Inputs from motor and premotor cortex to the superior colliculus of the macaque monkey. Behavioural Brain Research 18, 95–105, https://doi.org/10.1016/0166-4328(85)90066-X (1985).
doi: 10.1016/0166-4328(85)90066-X
pubmed: 3913446
Lang, P. J. et al. International affective picture system (IAPS): Affective ratings of pictures and instruction manual. Tech. Rep., University of Florida, Gainesville, FL (2008).
Vuilleumier, P. Affective and motivational control of vision. Current Opinion in Neurology 28, 29–35, https://doi.org/10.1097/WCO.0000000000000159 (2015).
doi: 10.1097/WCO.0000000000000159
pubmed: 25490197
Mulckhuyse, M. The influence of emotional stimuli on the oculomotor system: a review of the literature. Cognitive, Affective, & Behavioral Neuroscience 18, 411–425, https://doi.org/10.3758/s13415-018-0590-8 (2018).
doi: 10.3758/s13415-018-0590-8
Buhle, J. T. et al. Common representation of pain and negative emotion in the midbrain periaqueductal gray. Social Cognitive and Affective Neuroscience 8, 609–616, https://doi.org/10.1093/scan/nss038 (2013).
doi: 10.1093/scan/nss038
pubmed: 22446299
Mobbs, D. et al. Neural activity associated with monitoring the oscillating threat value of a tarantula. Proceedings of the National Academy of Sciences of the United States of America 107, 20582–6, https://doi.org/10.1073/pnas.1009076107 (2010).
doi: 10.1073/pnas.1009076107
pubmed: 21059963
pmcid: 2996708
Satpute, A. B. et al. Identification of discrete functional subregions of the human periaqueductal gray. Proceedings of the National Academy of Sciences of the United States of America 110, 17101–17106, https://doi.org/10.1073/pnas.1306095110 (2013).
doi: 10.1073/pnas.1306095110
pubmed: 24082116
pmcid: 3801046
Linnman, C., Moulton, E. A., Barmettler, G., Becerra, L. & Borsook, D. Neuroimaging of the periaqueductal gray: State of the field. NeuroImage 60, 505–22, https://doi.org/10.1016/j.neuroimage.2011.11.095 (2012).
doi: 10.1016/j.neuroimage.2011.11.095
pubmed: 22197740
Kober, H. et al. Functional grouping and cortical–subcortical interactions in emotion: A meta-analysis of neuroimaging studies. NeuroImage 42, 998–1031, https://doi.org/10.1016/j.neuroimage.2008.03.059 (2008).
doi: 10.1016/j.neuroimage.2008.03.059
pubmed: 18579414
pmcid: 2752702
LeDoux, J. Rethinking the emotional brain. Neuron 73, 653–676, https://doi.org/10.1016/J.NEURON.2012.02.004 (2012).
doi: 10.1016/J.NEURON.2012.02.004
pubmed: 22365542
pmcid: 3625946
Fanselow, M. S. Neural organization of the defensive behavior system responsible for fear. Psychonomic Bulletin & Review 1, 429–438, https://doi.org/10.3758/BF03210947 (1994).
doi: 10.3758/BF03210947
Bandler, R., Keay, K. A., Floyd, N. & Price, J. Central circuits mediating patterned autonomic activity during active vs. passive emotional coping. Brain research bulletin 53, 95–104 (2000).
doi: 10.1016/S0361-9230(00)00313-0
Satpute, A. B., Kragel, P. A., Barrett, L. F., Wager, T. D. & Bianciardi, M. Deconstructing arousal into wakeful, autonomic and affective varieties. Neuroscience Letters, https://doi.org/10.1016/J.NEULET.2018.01.042 (2018).
doi: 10.1016/j.neulet.2018.01.042
Vuilleumier, P., Armony, J. L., Driver, J. & Dolan, R. J. Effects of attention and emotion on face processing in the human brain: an event-related fMRI study. Neuron 30, 829–841, https://doi.org/10.1016/S0896-6273(01)00328-2 (2001).
doi: 10.1016/S0896-6273(01)00328-2
pubmed: 11430815
Vuilleumier, P., Armony, J. L., Driver, J. & Dolan, R. J. Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nature Neuroscience 6, 624–631, https://doi.org/10.1038/nn1057 (2003).
doi: 10.1038/nn1057
pubmed: 12740580
Morris, J. S., Ohman, A. & Dolan, R. J. A subcortical pathway to the right amygdala mediating unseen fear. Proceedings of the National Academy of Sciences of the United States of America 96, 1680–5, https://doi.org/10.1073/PNAS.96.4.1680 (1999).
doi: 10.1073/PNAS.96.4.1680
pubmed: 9990084
pmcid: 15559
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, https://doi.org/10.1093/brain/124.6.1241 (2001).
doi: 10.1093/brain/124.6.1241
pubmed: 11353739
Wei, P. et al. Processing of visually evoked innate fear by a non-canonical thalamic pathway. Nature Communications 6, 1–12, https://doi.org/10.1038/ncomms7756 (2015).
doi: 10.1038/ncomms7756
da Silva, J. A., Almada, R. C., de Figueiredo, R. M. & Coimbra, N. C. Blockade of synaptic activity in the neostriatum and activation of striatal efferent pathways produce opposite effects on panic attack-like defensive behaviours evoked by GABAergic disinhibition in the deep layers of the superior colliculus. Physiology & Behavior, https://doi.org/10.1016/j.physbeh.2018.07.021 (2018).
doi: 10.1016/j.physbeh.2018.07.021
Shang, C. et al. A parvalbumin-positive excitatory visual pathway to trigger fear responses in mice. Science 350, 198–204, https://doi.org/10.1126/science.aaa8694 (2015).
doi: 10.1126/science.aaa8694
Satpute, A. B. et al. Involvement of sensory regions in affective experience: a meta-analysis. Frontiers in Psychology 6, 1860, https://doi.org/10.3389/fpsyg.2015.01860 (2015).
doi: 10.3389/fpsyg.2015.01860
pubmed: 26696928
pmcid: 4678183
Chang, L. J., Gianaros, P. J., Manuck, S. B., Krishnan, A. & Wager, T. D. A sensitive and specific neural signature for picture-induced negative affect. PLoS Biology 13, e1002180, https://doi.org/10.1371/journal.pbio.1002180 (2015).
doi: 10.1371/journal.pbio.1002180
pubmed: 26098873
pmcid: 4476709
Damasio, A. & Carvalho, G. B. The nature of feelings: Evolutionary and neurobiological origins. Nature Reviews Neuroscience 14, 143–152, https://doi.org/10.1038/nrn3403 (2013).
doi: 10.1038/nrn3403
pubmed: 23329161
Shinkareva, S. V. et al. Representations of modality-specific affective processing for visual and auditory stimuli derived from functional magnetic resonance imaging data. Human Brain Mapping 35, 3558–3568, https://doi.org/10.1002/hbm.22421 (2014).
doi: 10.1002/hbm.22421
pubmed: 24302696
Miskovic, V., Kuntzelman, K., Chikazoe, J. & Anderson, A. K. Representation of affect in sensory cortex. Behavioral and Brain Sciences 39, e252, https://doi.org/10.1017/S0140525X15002708 (2016).
doi: 10.1017/S0140525X15002708
pubmed: 28355863
LeDoux, J. E. The Emotional Brain. (Simon & Schuster, New York, 1996).
Pessoa, L. & Adolphs, R. Emotion processing and the amygdala: from a ‘low road’ to ‘many roads’ of evaluating biological significance. Nature Reviews Neuroscience 11, 773–783, https://doi.org/10.1038/jid.2014.371 (2010).
doi: 10.1038/jid.2014.371
pubmed: 20959860
pmcid: 3025529
Hashemi, M. M. et al. Neural Dynamics of Shooting Decisions and the Switch from Freeze to Fight. Scientific Reports 9, 4240, https://doi.org/10.1038/s41598-019-40917-8 (2019).
doi: 10.1038/s41598-019-40917-8
pubmed: 30862811
pmcid: 6414631
Parr, T. & Friston, K. J. Active inference and the anatomy of oculomotion. Neuropsychologia 111, 334–343, https://doi.org/10.1016/J.NEUROPSYCHOLOGIA.2018.01.041 (2018).
doi: 10.1016/J.NEUROPSYCHOLOGIA.2018.01.041
pubmed: 29407941
pmcid: 5884328
Parr, T. & Friston, K. J. The Discrete and Continuous Brain: From Decisions to Movement—and Back Again. Neural Computation 1–29, https://doi.org/10.1162/NECO (2018).
Jenkinson, M., Beckmann, C. F., Behrens, T. E., Woolrich, M. W. & Smith, S. M. FSL. NeuroImage 62, 782–790, https://doi.org/10.1016/j.neuroimage.2011.09.015 (2012).
doi: 10.1016/j.neuroimage.2011.09.015
Woolrich, M. W. et al. Bayesian analysis of neuroimaging data in FSL. NeuroImage 45, S173–S186, https://doi.org/10.1016/j.neuroimage.2008.10.055 (2009).
doi: 10.1016/j.neuroimage.2008.10.055
pubmed: 19059349
Smith, S. M. et al. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23, S208–S219, https://doi.org/10.1016/j.neuroimage.2004.07.051 (2004).
doi: 10.1016/j.neuroimage.2004.07.051
pubmed: 15501092
Loureiro, J. R. et al. Depth-dependence of visual signals in the human superior colliculus at 9.4 T. Human Brain Mapping 38, 574–587, https://doi.org/10.1002/hbm.23404 (2016).
doi: 10.1002/hbm.23404
pubmed: 27659062
Naidich, T. P. et al. Duvernoy’s atlas of the human brain stem and cerebellum: High-field MRI: Surface anatomy, internal structure, vascularization and 3 D sectional anatomy (Springer Science & Business Media, 2009).
Wager, T. D., Keller, M. C., Lacey, S. C. & Jonides, J. Increased sensitivity in neuroimaging analyses using robust regression. NeuroImage 26, 99–113, https://doi.org/10.1016/j.neuroimage.2005.01.011 (2005).
doi: 10.1016/j.neuroimage.2005.01.011
pubmed: 15862210
Lakens, D. Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs. Frontiers in Psychology 4, https://doi.org/10.3389/fpsyg.2013.00863 (2013).
Rosenholtz, R., Li, Y. & Nakano, L. Measuring visual clutter. Journal of Vision 7, 17, https://doi.org/10.1167/7.2.17 (2007).
doi: 10.1167/7.2.17
pubmed: 18217832