Editorial Manager(tm) for Behavioral and Brain Sciences Manuscript Draft Manuscript Number: Title: Timing is a missing key ingredient in typical fMRI studies of emotion: A commentary on Lindquist et al. Short Title: Timing: A missing key ingredient in typical fMRI studies of emotion Article Type: Commentary Article Corresponding Author: Christian Waugh, Ph.D. Corresponding Author's Institution: Wake Forest University First Author: Christian Waugh, Ph.D. Order of Authors: Christian Waugh, Ph.D.;James Schirillo, PhD Abstract: Lindquist et al. provide a compelling summary of the brain bases of the onset of emotion. Their conclusions, however, are constrained by typical fMRI techniques that do not assess a key ingredient in emotional experience - timing. We discuss the importance of timing in theories of emotion as well as the implications of neural temporal dynamics for psychological constructionism.
Commentary Article Click here to download Commentary Article: Waugh_Schirillo_BBS_Commentary_Lindquist.doc
Target Article Authors: Kristen A. Lindquist, Tor D. Wager, Hedy Kober, Eliza Bliss-Moreau, and Lisa Feldman Barrett Word Count Abstract: 58 Main Text: 981 References: 299 Entire Text: 1338
Timing: A missing key ingredient in typical fMRI studies of emotion Christian E. Waugh1, James A. Schirillo2 Department of Psychology Wake Forest University
1,2
P.O. Box 7778, Winston Salem, NC 27109
1
To whom correspondence should be addressed:
[email protected], (336) 758-3631
2
[email protected]
Abstract Lindquist et al. provide a compelling summary of the brain bases of the onset of emotion. Their conclusions, however, are constrained by typical fMRI techniques that do not assess a key ingredient in emotional experience – timing. We discuss the importance of timing in theories of emotion as well as the implications of neural temporal dynamics for psychological constructionism.
Lindquist et al. advanced a very thoughtful review on the brain bases of emotion garnered from neuroimaging. Their summary should prove useful for investigators interested in understanding the functions of the brain regions involved with emotions. We also believe that the current state of neuroimaging evidence provides fairly compelling support for their psychological constructionist theory of emotions. We argue, however, that the current state of neuroimaging evidence, while necessary, is not sufficient to fully support their theory. Neuroimaging has thus far only provided a snapshot of the initial onset of emotion, while ignoring one of the most fundamental elements of emotional experience – time. Emotions happen over time. From the initial appraisal of an emotional event that can occur within hundreds of milliseconds (Schupp, et al., 2000) to event-induced moods that can endure for weeks (McCullough, Orsulak, Brandon, & Akers, 2007). Although often ignored empirically, time is an important parameter in most major theories of emotion. Process-models of emotion have emphasized that emotions endure and change over time, and that temporal approaches to understanding emotions should yield discoveries about how emotions are fundamentally processed (Larsen, Augustine, & Prizmic, 2009). For example, it has been shown that longer enduring emotional experiences can be predicted by the importance and initial intensity of the emotion-eliciting situation (Verduyn, Delvaux, Van Coillie, Tuerlinckx, & Van Mechelen, 2009). Beyond emotional reactivity, timing has also proved critical for understanding emotional regulation (Gross, 2001). Whether people enjoy the social, psychological, and physiological benefits of cognitive reappraisal (vs. suppression) depends, in part, on when they attempt to regulate their emotion (Gross, 2001). Finally, and particularly relevant to the current target article, it has been suggested that the timing of emotion is a key mechanism underlying the neural bases of individual differences in emotional experience (Davidson, 1998).
Despite the obvious importance of timing in understanding emotional experience, it has been mostly ignored in neuroimaging studies. The reason is simple: traditional functional magnetic resonance imaging (fMRI) statistical techniques do not estimate time. The overwhelming majority of fMRI analyses model the data with canonical gamma-based hemodynamic response functions (HRFs; Friston, Jezzard, & Turner, 1994). When these canonical HRFs are used to model the data, only one parameter – height – is allowed to vary. The temporal parameters of the HRF, such as the delay and dispersion, are typically fixed which does not allow for the estimation of possible temporal dynamics of the underlying blood oxygenation-level dependent (BOLD) response. There is a delay from neural activity to measurable BOLD response (Bandettini, Jesmanowicz, Wong, & Hyde, 1993), so these timeinvariant HRFs only assess hypothetical neural activity occurring in the first second after stimulus onset while failing to account for significantly delayed neural responses or neural responses of longer duration. This means that fMRI studies of emotion in large part fail to capture the development of emotional experience beyond the initial response to the emotional stimulus. Recent studies that have used time-varying HRFs show why estimating temporal features of the BOLD response may prove critical to test Lindquist et al.’s conclusions. In one study, we used the summation of three inverse-logit curves as a time-varying HRF (Lindquist & Wager, 2007) to examine how the duration of BOLD activity relates to self-reported intensity of emotional experience (Waugh, Hamilton, & Gotlib, 2010). First, we found that the insula exhibited extended duration of BOLD activity to more intense negative images. Lindquist et al. proposed that the insula, as part of the core affect network, represents visceral arousal. This suggests that although visceral arousal can occur quickly, it can also be sustained for a
significant period of time and, perhaps, lead to sustained insula activation. Second, we found that regions along the cortical midline, the medial prefrontal cortex (mPFC) and posterior cingulate (PCC), also exhibited extended duration of BOLD activity to intense negative images. In conjunction with Lindquist et al.’s proposal that these regions are associated with the situated conceptualization of emotional experiences, this finding suggests that in intense emotional situations these structures may stay online to continually monitor the meaning of the situation to the self. Indeed, in another study examining neural responses during long periods (~2 minutes) of social evaluative threat the mPFC was found to stay active for the entire duration of the stress period (Wager, et al., 2009). These findings that the insula and cortical midline exhibit extended duration of activation during intense emotion offer an example of how estimating timing of emotion could support or challenge Lindquist et al.’s psychological constructionist argument. One supporting argument would be that each of these regions may be responsible for certain psychological constructs that, although enduring over time, do not fundamentally change. Thus, a snapshot of an emotion at any time point after the initial onset could still be a construction of these separable constructs. A potential challenge to this argument would be that these systems do behave very differently over time. Although the ‘making meaning’ function of the cortical midline regions may persist over time, the very meaning that this system generates may qualitatively change. Through these shifts in meaning, the cortical midline could alter the network of active regions by selectively enhancing or reducing the input from regions according to the relevance of their associated psychological constructs to the meaning being made about the situation. For example, the network of constructs associated with the initial response to a potential anger-eliciting situation
(e.g. salience, attention, motivation) may, over time, become shaped to correspond to the increasing ‘anger-ness’ of the situation (e.g., motivation, agency). The above formulations are quite speculative; indeed, it is even unclear whether, if correct, they would support or not Lindquist et al’s constructionist argument. Our purpose in presenting them was merely to emphasize the importance of assessing temporal characteristics of neural responses to emotion. Emotions develop over time, and understanding precisely how they do so will greatly improve our understanding of how they are constructed in the brain.
References Bandettini, P. A., Jesmanowicz, A., Wong, E. C., & Hyde, J. S. (1993). Processing strategies for time-course data sets in functional mri of the human brain. Magnetic Resonance in Medicine, 30(2), 161-173. Davidson, R. J. (1998). Affective style and affective disorders: Perspectives from affective neuroscience. Cognition and Emotion, 12, 307-330. Friston, K. J., Jezzard, P., & Turner, R. (1994). Analysis of functional MRI time-series. Human Brain Mapping, 1(2), 153-171. Gross, J. J. (2001). Emotion regulation in adulthood: Timing is everything. Current Directions in Psychological Science, 10(6), 214-219. Larsen, R. J., Augustine, A. A., & Prizmic, Z. (2009). A process approach to emotion and personality: Using time as a facet of data. Cognition & Emotion, 23(7), 1407-1426. Lindquist, M. A., & Wager, T. D. (2007). Validity and power in hemodynamic response modeling: A comparison study and a new approach. Human Brain Mapping, 28(8), 764784. McCullough, M. E., Orsulak, P., Brandon, A., & Akers, L. (2007). Rumination, fear, and cortisol: An in vivo study of interpersonal transgressions. Health Psychology, 26(1), 126132. Schupp, H. T., Cuthbert, B. N., Bradley, M. M., Cacioppo, J. T., Ito, T., & Lang, P. J. (2000). Affective picture processing: The late positive potential is modulated by motivational relevance. Psychophysiology, 37, 257-261.
Verduyn, P., Delvaux, E., Van Coillie, H., Tuerlinckx, F., & Van Mechelen, I. (2009). Predicting the duration of emotional experience: Two experience sampling studies. Emotion, 9(1), 83-91. Wager, T. D., Waugh, C. E., Lindquist, M., Noll, D. C., Fredrickson, B. L., & Taylor, S. F. (2009). Brain mediators of cardiovascular responses to social threat, Part I: Reciprocal dorsal and ventral sub-regions of the medial prefrontal cortex and heart-rate reactivity. Neuroimage, 47, 821-835. Waugh, C. E., Hamilton, J. P., & Gotlib, I. H. (2010). The neural temporal dynamics of the intensity of emotional experience. Neuroimage, 49, 1699-1707.
