Episodic simulation; Future thinking; Mental time travel; Neuropsychology; Pulvinar
Abstract :
[en] The pulvinar nucleus represents a key neural structure involved in signalling emotional content in the domain of visual perception, whereas its role in the processing of simulated emotional events is less clear. fMRI research has hinted at a role for the pulvinar in imagined emotional scenarios, but the evidence is mixed and this proposal has yet to be tested using the lesion study method. In this study, 3 patients with unilateral lesions to the pulvinar, and 10 matched control participants, completed a set of well-established tasks that required them to think about emotional past and future events. This procedure allowed for a comprehensive evaluation of emotional past and future thinking, using both subjective and objective measures. The results indicate that, relative to controls, processing of emotional past and future events is not impaired in patients with unilateral pulvinar nucleus lesions. However, outcomes of this study should be interpreted in the context of the volume, lateralisation and location of pulvinar lesions in these cases. These data have implications for understanding of the processing of emotionally-salient stimuli in the context of pulvinar damage.
Disciplines :
Neurosciences & behavior
Author, co-author :
Cole, Scott ; York St John University, United Kingdom. Electronic address: s.cole1@yorksj.ac.uk
Szpunar, Karl; Toronto Metropolitan University, Toronto, United Kingdom
Benoit, Roland; University of Colorado, Boulder, United Kingdom
Addis, D.R., Wong, A.T., Schacter, D.L., Remembering the past and imagining the future: Common and distinct neural substrates during event construction and elaboration. Neuropsychologia 45:7 (2007), 1363–1377, 10.1016/j.neuropsychologia.2006.10.016.
Addis, D.R., Wong, A.T., Schacter, D.L., Age-Related changes in the episodic simulation of future events. Psychological Science 19:1 (2008), 33–41, 10.1111/j.1467-9280.2008.02043.x.
Andrade, J., Ijdema, T., Vadasz, N., May, J., Tell me all about it: Narrated memories are less emotional than imagined memories. The Quarterly Journal of Experimental Psychology: QJEP 76:7 (2023), 1683–1695, 10.1177/17470218221126720 2006.
Arend, I., Rafal, R., Ward, R., Spatial and temporal deficits are regionally dissociable in patients with pulvinar lesions. Brain: a Journal of Neurology 131:8 (2008), 2140–2152.
Barron, D.D., Eickhoff, S.B., Clos, M., Fox, P.T., Human pulvinar functional organization and connectivity. Human Brain Mapping 36:7 (2015), 2417–2431, 10.1002/hbm.22781.
Barron, H.C., Garvert, M.M., Behrens, T.E., Repetition suppression: A means to index neural representations using BOLD?. Philosophical Transactions of the Royal Society B, 371(1705), 2016, 20150355, 10.1098/rstb.2015.0355.
Barsics, C., Van Der Linden, M., D'Argembeau, A., Frequency, characteristics, and perceived functions of emotional future thinking in daily life. The Quarterly Journal of Experimental Psychology: QJEP 69:2 (2016), 217–233, 10.1080/17470218.2015.1051560.
Benoit, R.G., Schacter, D.L., Specifying the core network supporting episodic simulation and episodic memory by activation likelihood estimation. Neuropsychologia 75 (2015), 450–457, 10.1016/j.neuropsychologia.2015.06.034.
Berntsen, D., Rubin, D.T., Pretraumatic stress reactions in soldiers deployed to Afghanistan. Clinical Psychological Science 3:5 (2015), 663–674, 10.1177/2167702614551766.
Berntsen, D., Rubin, D.T., Salgado, S., The frequency of involuntary autobiographical memories and future thoughts in relation to daydreaming, emotional distress, and age. Consciousness and Cognition 36 (2015), 352–372, 10.1016/j.concog.2015.07.007.
Bub, D.N., Methodological issues confronting PET and fMRI studies of cognitive function. Cognitive Neuropsychology 17 (2000), 467–484.
Burton, H., Jones, E.G., The posterior thalamic region and its cortical projection in New World and Old World monkeys. The Journal of Comparative Neurology 168:2 (1976), 249–301, 10.1002/cne.901680204.
Caramazza, A., The logic of neuropsychological research and the problem of patient classification in aphasia. Brain and Language 21:1 (1984), 9–20, 10.1016/0093-934X(84)90032-4.
Ciaramelli, E., De Luca, F., Kwan, D., Mok, J., Bianconi, F., Knyagnytska, V., Craver, C., Green, L., Myerson, J., Rosenbaum, R.S., The role of ventromedial prefrontal cortex in reward valuation and future thinking during intertemporal choice. eLife, 10, 2021, e67387, 10.7554/eLife.67387.
Cole, S., Pulvinar damage case series. https://doi.org/10.17605/OSF.IO/ZKDS3, 2023.
Cole, S.N., Fotopoulou, A., Oddy, M., Moulin, C.J., Implausible future events in a confabulating patient with an anterior communicating artery aneurysm. Neurocase 20:2 (2014), 208–224, 10.1080/13554794.2012.741259.
Cole, S.N., Morrison, C.M., Conway, M.A., Episodic future thinking: Linking neuropsychological performance with episodic detail in young and old adults. The Quarterly Journal of Experimental Psychology: QJEP 66:9 (2013), 1687–1706.
Cole, S.N., Staugaard, S., Berntsen, D., Inducing involuntary and voluntary mental time travel using a laboratory paradigm. Memory and Cognition 44 (2016), 376–389, 10.3758/s13421-015-0564-9.
Crawford, J.R., Garthwaite, P.H., Porter, S., Point and interval estimates of effect sizes for the case-controls design in neuropsychology: Rationale, methods, implementations, and proposed reporting standards. Cognitive Neuropsychology 27 (2010), 245–260, 10.1080/02643294.2010.513967.
Crawford, J.R., Garthwaite, P.H., Ryan, K., Comparing a single case to a control sample: Testing for neuropsychological deficits and dissociations in the presence of covariates. Cortex; a Journal Devoted To the Study of the Nervous System and Behavior 47 (2011), 1166–1178.
D'Argembeau, A., Van der Linden, M., Phenomenal characteristics associated with projecting oneself back into the past and forward into the future: Influence of valence and temporal distance. Consciousness and Cognition 13:4 (2004), 844–858, 10.1016/j.concog.2004.07.007.
Danziger, S., Ward, R., Owen, V., Rafal, R.D., Contributions of the human pulvinar to linking vision and action. Cognitive, Affective, & Behavioral Neuroscience 4:1 (2004), 89–99, 10.3758/cabn.4.1.89.
Devitt, A.L., Thakral, P.P., Szpunar, K.K., Addis, D.R., Schacter, D.L., Age-related changes in repetition suppression of neural activity during emotional future simulation. Neurobiology of Aging 94 (2020), 287–297, 10.1016/j.neurobiolaging.2020.06.016.
Dritschel, B.H., Williams, J.M.G., Baddeley, A.D., Nimmo-Smith, I., Autobiographical fluency: A method for the study of personal memory. Memory & Cognition 20 (1992), 133–140.
Gross, J.J., Carstensen, L.L., Pasupathi, M., Tsai, J., Götestam Skorpen, C., Hsu, A.Y., Emotion and aging: experience, expression, and control. Psychology and aging, 12(4), 1997, 590, 10.1037//0882-7974.12.4.590.
Guedj, C., Vuilleumier, P., Functional connectivity fingerprints of the human pulvinar: Decoding its role in cognition. Neuroimage, 221, 2020, 117162, 10.1016/j.neuroimage.2020.117162.
Koo, T.K., Li, M.Y., A guideline of selecting and reporting Intraclass correlation coefficients for reliability research. Journal of Chiropractic Medicine 15:2 (2016), 155–163, 10.1016/j.jcm.2016.02.012.
Levine, B., Svoboda, E., Hay, J.F., Winocur, G., Moscovitch, M., Aging and autobiographical memory: Dissociating episodic from semantic retrieval. Psychology and Aging 17:4 (2002), 677–689.
Liebermann, D., Ostendorf, F., Kopp, U.A., Kraft, A., Bohner, G., Nabavi, D.G., Ploner, C.J., Subjective cognitive-affective status following thalamic stroke. Journal of Neurology 260 (2013), 386–396.
MacLeod, A.K., Rose, G.S., Williams, J.M.G., Components of hopelessness about the future in parasuicide. Cognitive Therapy and Research 17 (1993), 441–455.
Marsh, L., Edginton, T., Conway, M.A., Loveday, C., Positivity bias in past and future episodic thinking: Relationship with anxiety, depression, and retrieval-induced forgetting. Quarterly Journal of Experimental Psychology 72:3 (2018), 508–522, 10.1177/1747021818758620.
Morel, A., Magnin, M., Jeanmonod, D., Multiarchitectonic and stereotactic atlas of the human thalamus. Journal of Comparative Neurology 387:pg (1997), 588–630.
Najdenovska, E., Alemán-Gómez, Y., Battistella, G., Descoteaux, M., Hagmann, P., Jacquemont, S., Bach Cuadra, M., In-vivo probabilistic atlas of human thalamic nuclei based on diffusion- weighted magnetic resonance imaging. Scientific Data, 5, 2018, 180270, 10.1038/sdata.2018.270.
Nickels, L., Howard, D., Best, W., On the use of different methodologies in cognitive neuropsychology: Drink deep and from several sources. Cognitive Neuropsychology 28:7 (2011), 475–485.
Pergola, G., Danet, L., Pitel, A.L., Carlesimo, G.A., Segobin, S., Pariente, J., Suchan, B., Mitchell, A.S., Barbeau, E.J., The regulatory role of the human mediodorsal thalamus. Trends in Cognitive Sciences 22:11 (2018), 1011–1025, 10.1016/j.tics.2018.08.006.
Pessoa, L., Adolphs, R., Emotion processing and the amygdala: From a ‘low road’ to ‘many roads’ of evaluating biological significance. Nature reviews. Neuroscience 11:11 (2010), 773–783, 10.1038/nrn2920.
Rafal, R.D., Koller, K., Bultitude, J.H., Mullins, P.R., Ward, R., Mitchell, A., Bell, A.J., Connectivity between the superior colliculus and the amygdala in humans and macaque monkeys: Virtual dissection with probabilistic DTI tractography. Journal of Neurophysiology 114:3 (2015), 1947–1962, 10.1152/jn.01016.2014.
Rasmussen, K.L., Berntsen, D., Autobiographical memory and episodic future thinking after moderate to severe traumatic brain injury. Journal of Neuropsychology 8:1 (2014), 34–52, 10.1111/jnp.12003.
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. Journal of Comparative Neurology 379:3 (1997), 313–332.
Schacter, D.L., Addis, D.R., Hassabis, D., Martin, V.C., Spreng, R.N., Szpunar, K.K., The future of memory: Remembering, imagining, and the brain. Neuron 76:4 (2012), 677–694, 10.1016/j.neuron.2012.11.001.
Shallice, T., Cognitive neuropsychology and its vicissitudes: The fate of Caramazza's axioms. Cognitive Neuropsychology 32:7–8 (2015), 385–411, 10.1080/02643294.2015.1131677.
Shrikanth, S., Szpunar, P.M., Szpunar, K.K., Staying positive in a dystopian future: A novel dissociation between personal and collective cognition. Journal of Experimental Psychology: General 147:8 (2018), 1200–1210, 10.1037/xge0000421.
Szpunar, K.K., Jing, H.G., Benoit, R.G., Schacter, D.L., Repetition-related reductions in neural activity during emotional simulations of future events. Plos One, 10(9), 2015, e0138354, 10.1371/journal.pone.0138354.
Tamietto, M., De Gelder, B., Neural bases of the non-conscious perception of emotional signals. Nature Reviews Neuroscience 11:10 (2010), 697–709.
Tulving, E., Episodic memory: From mind to brain. Annual Review of Psychology 53 (2002), 1–25, 10.1146/annurev.psych.53.100901.135114.
Turnbull, O.H., Cognitive neuropsychology comes of age: A review of B. Rapp (2001). Handbook of cognitive neuropsychology. Cortex; a Journal Devoted To the Study of the Nervous System and Behavior 37 (2001), 445–450.
Turnbull, O.H., Evans, C.E., Owen, V., Negative emotions and anosognosia. Cortex; a Journal Devoted To the Study of the Nervous System and Behavior 41:1 (2005), 67–75, 10.1016/s0010-9452(08)70179-5.
Vaidya, A.R., Pujara, M.S., Petrides, M., Murray, E.A., Fellows, L.K., Lesion studies in contemporary neuroscience. Trends in Cognitive Sciences, 23(8), 2019, 10.1016/j.tics.2019.05.009.
Ward, R., Calder, A.J., Parker, M., Arend, I., Emotion recognition following human pulvinar damage. Neuropsychologia 45:8 (2007), 1973–1978, 10.1016/j.neuropsychologia.2006.09.017.
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 Neuroscience 5:2 (2002), 99–100.
Williams, J.C., Ellis, N.C., Tyers, C., Healy, H., Rose, G., MacLeod, A.M., The specificity of autobiographical memory and imageability of the future. Memory & Cognition 24:1 (1996), 116–125, 10.3758/bf03197278.
Young, K., Bonkale, W., Holcomb, L., Hicks, P., German, D., Major depression, 5HTTLPR genotype, suicide and antidepressant influences on thalamic volume. The British Journal of Psychiatry 192:4 (2008), 285–289, 10.1192/bjp.bp.107.039180.
Yushkevich, P.A., Yang, G., Gerig, G., ITK-SNAP: An interactive tool for semi-automatic segmentation of multi-modality biomedical images. Annual International Conference of the IEEE Engineering in Medicine and Biology Society, 2016, 3342–3345, 10.1109/embc.2016.7591443.
Zigmond, A.S., Snaith, R.P., The hospital anxiety and Depression scale. Acta Psychiatrica Scandinavica 67:6 (1983), 361–370, 10.1111/j.1600-0447.1983.tb09716.x.