Neural Mechanisms Behind the Effects of Tactile False Feedback on Emotion Perception

Poster No:

745 

Submission Type:

Abstract Submission 

Authors:

Joel Patchitt1, Hugo Critchley1, Mark Miller2, Manos Tsakiris3, Sarah Garfinkel4, Andy Clark5

Institutions:

1Brighton and Sussex Medical School, Brighton, East Sussex, 2University of Edinburgh, Edinburgh, The City of Edinburgh, 3Royal Holloway, Egham, Surrey, 4University College London, London, Greater London, 5University of Sussex, Brighton, East Sussex

First Author:

Joel Patchitt  
Brighton and Sussex Medical School
Brighton, East Sussex

Co-Author(s):

Hugo Critchley, Professor  
Brighton and Sussex Medical School
Brighton, East Sussex
Mark Miller, Dr  
University of Edinburgh
Edinburgh, The City of Edinburgh
Manos Tsakiris, Professor  
Royal Holloway
Egham, Surrey
Sarah Garfinkel, Professor  
University College London
London, Greater London
Andy Clark, Professor  
University of Sussex
Brighton, East Sussex

Introduction:

Bi-directional mismatches between perceived and veridical physiological signals during false physiological feedback (FFB) exerts subtle effects on ambiguous emotional judgements (Valins, 1966; Gray et al., 2007). The determinants of these effects are proposed to be reliant on the conscious appraisal of interoceptive information (Crucian et al., 2000; Gray et al., 2007). Most paradigms use auditory FFB, finding increases in emotional intensity ratings, irrespective of FFB direction (Valins, 1966; Gray., et al, 2007), with right anterior insula (rAI) serving as a mismatch comparator (Critchley., et al, 2004; Gray et al., 2007). Few paradigms have looked at the effects of tactile FFB, which could be interpreted as a more veridical sensation of HR. We hypothesized that tactile FFB would be interpreted as a veridical physiological signal, with increased FFB activating the rAI and other socio-emotional regions, resulting in bi-directional effects on emotional face ratings.

Methods:

During fMRI BOLD acquisition using a Siemens 3T scanner, 41 participants performed a simple emotional intensity rating task in which 80 faces (positive/negative) biased towards neutral were shown and repeated for four conditions of vibro-tactile FFB stimulation on the right wrist (Higher than HR, lower than HR, same HR, No FFB). Conditions changed and repeated every five trials totalling 20 seconds per block. A linear mixed model analysis (LMM) was conducted on the behavioural data: Condition (Higher, Lower, Null), Valance (Positive, Negative) and Trial (1-5). Data was pre-processed using fMRIPrep and analysed in FSL. Contrasts were run for A) feedback of any type vs no feedback B) Higher FFB vs Lower FFB C) Interaction between FFB (Higher, Lower) and Valance (Positive v Negative).

Results:

We found a three way interaction between Condition, Valance and Trial F(2) = 49.792, p = <0.001 (see fig 1). Bonferroni corrected Post hoc LMM revealed an interaction between Valance and Trial in the Higher F(1) = 62.185, p = <0.00 and Lower F(1) = 39.375, p = <0.001 conditions but not for Null F(1) = 0.14, p = .708.
Correlations were found for: Contrast A in the left dorsal pre-motor cortex (lPMd), bilateral OP1, right dorsal posterior insula (rPId) and right primary sensorimotor cortex/corticospinal tract (rSMI), Contrast B in the rPId, middle (rMId) and anterior insula (rAId), right pars opercularis (rPOp) and pars orbitalis (rPOr), right superior temporal gyrus (rSTGs), inferior supramarginal gyrus (rSMGs) and bilateral occipital fusiform gyrus (OFG) and Contrast C in the left OP1.
Supporting Image: behavioural.png
   ·Fig 1. Three way interaction between FFB Condition, Emotion and Trial. FFB at higher than HR increases emotional intensity ratings over time and FFB at lower than HR decreases intensity ratings.
Supporting Image: highervslower.png
   ·Fig 2. Imaging contrast of FFB higher than HR vs lower than HR. Acitvation across dorsal Posterior Middle and Anterior Insula, Inferior Frontal Cortex, Superior Temporal and Occipital Fusiform Gyri.
 

Conclusions:

Behavioural results suggest a bi-directional exposure effect of FFB on subjective intensity ratings of emotionally ambiguous faces. This mimics the effect of arousal on emotional decision making, suggesting that tactile FFB is treated as a veridical interoceptive afferent. Bilateral OP1 and rPId suggest that FFB signals are ascending via c-type fibres as part of an affective touch pathway (Morrison et al., 2016), upon which a body ownership vs threat to peri-personal space decision is made in the lPMv (Bekrater-Bodmann et al., 2011). Activation within regions relating to body ownership (rPId, rMId, lPMv) suggest that FFB is integrated as a bodily owned percept (Tsakiris et al., 2007), potentially suppressing defensive reflexes via transcallosal pathways between the lPMv and rSMI (Bestmann et al., 2007). Activations across rAId and other regions in Contrast C suggest an effect of FFB across a socio-emotional network related to interoceptively induced changes emotion perception (Xu et al., 2021). Interaction between FFB and emotion in the contralateral OP1 suggests multimodal integration of sensory stimuli affecting prior bias in perceptual decision making (Preuschoff et al., 2010). This data highlights the potential of tactile feedback at biasing emotionally charged perceptual decisions and provides insight into the neural mechanisms by which interoceptive channels exert this bias.

Emotion, Motivation and Social Neuroscience:

Emotional Perception 1
Social Cognition

Modeling and Analysis Methods:

Activation (eg. BOLD task-fMRI)

Perception, Attention and Motor Behavior:

Perception: Pain and Visceral 2
Perception: Tactile/Somatosensory

Keywords:

Affective Disorders
Autonomics
Emotions
FUNCTIONAL MRI
Perception
Somatosensory
Other - Interoception; False Feedback; Tactile

1|2Indicates the priority used for review

Provide references using author date format

Bekrater-Bodmann, R., Foell, J., & Kamping, S. (2011). The importance of ventral premotor cortex for body ownership processing. Journal of Neuroscience, 31(26), 9443–9444. https://doi.org/10.1523/jneurosci.2302-11.2011
Bestmann, S., Swayne, O., Blankenburg, F., Ruff, C. C., Haggard, P., Weiskopf, N., Josephs, O., Driver, J., Rothwell, J. C., & Ward, N. S. (2007). Dorsal premotor cortex exerts state-dependent causal influences on activity in contralateral primary motor and dorsal premotor cortex. Cerebral Cortex, 18(6), 1281–1291. https://doi.org/10.1093/cercor/bhm159
Critchley, H. D., Wiens, S., Rotshtein, P., Öhman, A., & Dolan, R. J. (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience, 7(2), Article 2. https://doi.org/10.1038/nn1176
Crucian, G. P., Hughes, J. D., Barrett, A. M., Williamson, D. J. G., Bauer, R. M., Bowers, D., & Heilman, K. M. (2000). Emotional and Physiological Responses to False Feedback* *This paper was presented in part at the 27th annual meeting of the International Neuropsychological Society, Boston, MA, February, 1999. Cortex, 36(5), 623–647. https://doi.org/10.1016/S0010-9452(08)70542-2
Gray, M. A., Harrison, N. A., Wiens, S., & Critchley, H. D. (2007). Modulation of Emotional Appraisal by False Physiological Feedback during fMRI. PLOS ONE, 2(6), e546. https://doi.org/10.1371/journal.pone.0000546
Morrison, I. (2016). Ale Meta‐analysis reveals dissociable networks for affective and discriminative aspects of touch. Human Brain Mapping, 37(4), 1308–1320. https://doi.org/10.1002/hbm.23103
Preuschhof, C., Schubert, T., Villringer, A., & Heekeren, H. R. (2010). Prior information biases stimulus representations during vibrotactile decision making. Journal of Cognitive Neuroscience, 22(5), 875–887. https://doi.org/10.1162/jocn.2009.21260
Tsakiris, M., Hesse, M. D., Boy, C., Haggard, P., & Fink, G. R. (2006). Neural signatures of body ownership: A sensory network for bodily self-consciousness. Cerebral Cortex, 17(10), 2235–2244. https://doi.org/10.1093/cercor/bhl131
Valins, S. (1966). Cognitive effects of false heart-rate feedback. Journal of Personality and Social Psychology, 4(4), 400. https://doi.org/10.1037/h0023791
Xu, P., Peng, S., Luo, Y., & Gong, G. (2021). Facial expression recognition: A meta-analytic review of theoretical models and neuroimaging evidence. Neuroscience & Biobehavioral Reviews, 127, 820–836. https://doi.org/10.1016/j.neubiorev.2021.05.023