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Functional asymmetry and interhemispheric cooperation in the perception of emotions from facial expressions

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Abstract

The present study used the redundant target paradigm on healthy subjects to investigate functional hemispheric asymmetries and interhemispheric cooperation in the perception of emotions from faces. In Experiment 1 participants responded to checkerboards presented either unilaterally to the left (LVF) or right visual half field (RVF), or simultaneously to both hemifields (BVF), while performing a pointing task for the control of eye movements. As previously reported (Miniussi et al. in J Cogn Neurosci 10:216–230, 1998), redundant stimulation led to shorter latencies for stimulus detection (bilateral gain or redundant target effect, RTE) that exceeded the limit for a probabilistic interpretation, thereby validating the pointing procedure and supporting interhemispheric cooperation. In Experiment 2 the same pointing procedure was used in a go/no-go task requiring subjects to respond when seeing a target emotional expression (happy or fearful, counterbalanced between blocks). Faster reaction times to unilateral LVF than RVF emotions, regardless of valence, indicate that the perception of positive and negative emotional faces is lateralized toward the right hemisphere. Simultaneous presentation of two congruent emotional faces, either happy or fearful, produced an RTE that cannot be explained by probability summation and suggests interhemispheric cooperation and neural summation. No such effect was present with BVF incongruent facial expressions. In Experiment 3 we studied whether the RTE for emotional faces depends on the physical identity between BVF stimuli, and we set a second BVF congruent condition in which there was only emotional but not physical or gender identity between stimuli (i.e. two different faces expressing the same emotion). The RTE and interhemispheric cooperation were present also in this second BVF congruent condition. This shows that emotional congruency is the sufficient condition for the RTE to take place in the intact brain and that the cerebral hemispheres can interact in spite of physical differences between stimuli.

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Notes

  1. In principle, the RTE and the violation of the inequality test in Experiment 3 might be consistent also with the interactive race model put forth by Mordkoff and Yantis (1991), and not only with neural coactivation and interhemispheric summation. Indeed, since both the BVF conditions in go trials were congruent (i.e. a BVF incongruent condition with one target and one non-target was lacking in this experiment), Experiment 3 introduced contingencies among stimulus events that were absent in Experiment 2 and that might have favoured the RTE and inequality violations. To test whether our participants were, in fact, sensitive to these contingencies, we performed a direct comparison of the mean RTs between identical conditions in Experiment 2 (free of biased contingencies) and 3 (i.e. LVF, RVF, and BVF congruent identity conditions). Thus, we conducted a 2×2×3 ANOVA with the between-subjects factor of experiment (Exp. 2 vs. Exp. 3) and the within-subjects factors of facial expression (happy vs. fearful) and stimulus condition (unilateral LVF, RVF, and BVF congruent identity). The results showed a significant main effect of facial expression [F(1,43)=45.51, P<0.0001] and stimulus condition [F(2,86)=30.99, P<0.0001]. Importantly, the main effect of experiment [F(1,43)=0.035, P>0.85] and the experiment × facial expression [F(1,43)=0.03, P>0.86], experiment × stimulus condition [F(2,86)=0.31, P>0.73] and experiment × facial expression × stimulus condition [F(2,86)=0.06, P>0.93] interactions were all non-significant, with the largest difference between comparable conditions in Experiment 2 and 3 equal to 5.44 ms. This clearly indicates that the potentially useful information in favour of an enhanced bilateral gain present in Experiment 3 was not actually used by our subjects who performed as in Experiment 2 free of biased contingencies. Thus, even in this third experiment, the RTE and the violation of the inequality test in both the BVF conditions is likely to be the result of neural coactivation and interhemispheric summation rather than of interactive separate activation.

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Acknowledgements

This work was supported by a grant from the Ordine Mauriziano di Torino to M. Tamietto. We wish to warmly thank Silvia Savazzi for her valuable comments and help in computing the CDFs for the inequality test. Thanks are due to the anonymous Reviewer 1 for the helpful remarks and critiques. Thanks also to Sonia Cosentino and Emanuela Rocci for their support in testing and to Silvia Testa for help in data analysis.

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  1. Department of Psychology and Center for Cognitive Science, University of Turin, Via Po 14, 10123, Turin, Italy

    Marco Tamietto, Luca Latini Corazzini & Giuliano Geminiani

  2. Cognitive and Affective Neurosciences Laboratory, Tilburg University, Tilburg, The Netherlands

    Beatrice de Gelder

  3. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA, USA

    Beatrice de Gelder

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  1. Marco Tamietto
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  2. Luca Latini Corazzini
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Correspondence to Marco Tamietto.

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This work was supported by a grant from the Ordine Mauriziano di Torino to M.Tamietto.

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Tamietto, M., Latini Corazzini, L., de Gelder, B. et al. Functional asymmetry and interhemispheric cooperation in the perception of emotions from facial expressions. Exp Brain Res 171, 389–404 (2006). https://doi.org/10.1007/s00221-005-0279-4

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