States of mind: Emotions, body feelings, and thoughts share distributed neural networks
Highlights
► We report a novel study testing a constructionist model of the mind. ► Following scenarios, participants generated body feelings, emotions, or thoughts. ► Activity within distributed brain networks was measured using fMRI. ► All mental states involved activity in the same distributed brain networks. ► Relative differences in brain networks occurred between mental states.
Introduction
During every waking moment of life, a human mind consists of a variety of mental states. These mental states are typically named in commonsense terms, such as emotions (e.g., fear, disgust, love), cognitions (e.g., retrieving a memory, planning the future, concentrating on a task), perceptions (e.g., face perception, color perception, sound perception), and so on. Since the beginning of psychological science, researchers have assumed that each of these words refers to a separate and distinct kind of mental category or “faculty” (Lindquist and Barrett, under review, Uttal, 2001). Accordingly, scientists have searched for the physical correlates of these mental categories for over a century—in behavior, in peripheral physiology, and most recently, in a functioning brain. For example, cognitive neuroscientists have attempted to identify the unified neural basis of fear (e.g., Whalen et al., 1998), disgust (e.g., Wicker et al., 2003), love (e.g., Bartels and Zeki, 2000), the self (e.g., Northoff and Bermpohl, 2004), episodic memory (Rugg et al., 2002), semantic memory (e.g., Grossman et al., 2002), working memory (e.g., D'Esposito et al., 1998), face perception (e.g., Kanwisher et al., 1997) and so on. Twenty years of neuroimaging research is revealing, however, that the brain does not respect faculty psychology categories (Barrett, 2009, Duncan and Barrett, 2007, Gonsalves and Cohen, 2010, Lindquist and Barrett, under review, Lindquist et al., 2012b, Pessoa, 2008, Poldrack, 2010, Uttal, 2001).
Instead of revealing domain-specific brain areas that are specific to each mental faculty, growing evidence points to the hypothesis that diverse mental states emerge from the combination of domain-general psychological processes or “ingredients” that map to large-scale distributed networks in association regions of the brain (cf., Barrett, 2009, Barrett, 2011). In psychology, there is a theoretical tradition for hypothesizing that mental states emerge from the combination of more basic, domain-general, psychological processes—it is known as a constructionist approach. Throughout the past century, the constructionist approach has been most popular in models of emotion (e.g., Barrett, 2006, Barrett, 2012, Harlow and Stagner, 1932, Lindquist et al., 2012b, Russell, 2003, Schachter and Singer, 1962; for a review see, Gendron and Barrett, 2009), although its roots can be found in the earliest psychological writing (Dewey, 1895, James, 1890, Wundt, 1897/1998). The essence of a constructionist approach is the idea that during every moment of waking life, the brain constructs mental states such as emotions, body states, and thoughts by creating situated conceptualizations (Barrett, 2006, Barsalou, 2009) that combine three sources of stimulation: sensory stimulation from the world outside the skin (the exteroceptive sensory array of light and vibrations and chemicals and so on), sensory signals from within the body (somatovisceral stimulation, also called the interoceptive sensory array or the “internal milieu”), and prior experience (also referred to as memory or category knowledge that the brain makes available in part by the re-activation of sensory and motor neurons). These three sources – sensations from the world, sensations from the body, and prior experience – are continually available and the brain networks that process them might be thought of as part of the basic ingredients that form all mental life. Different “recipes” (the combination and weighting of the ingredients) are hypothesized to produce the myriad mental events that people give commonsense names (i.e., “emotions”, “cognitions”, and “perceptions”). From this perspective, mental categories such as emotions, cognitions, and perceptions are populated by a diverse set of instances that are events to explain, not specific causal processes linked to specific brain regions or networks.
There are three lines of work that support a constructionist functional architecture of mental states. First, there is a growing appreciation in the neuroimaging literature that the same networks have increased activation across a variety of different psychological task domains. For instance, the “default network”, including regions of the medial prefrontal cortex, medial temporal lobe, and posterior cingulate cortex, has increased activation during emotion (e.g., Lindquist et al., 2012b), emotion regulation (e.g., Wager et al., 2008b), representation of the self (e.g., Kelley et al., 2002), mental state attribution to others (e.g., Mitchell et al., 2005), moral reasoning (e.g., Young et al., 2011), episodic memory and prospection (e.g., Addis et al., 2007), semantic processing (e.g., Binder et al., 2009), and even context-sensitive visual perception (Bar et al., 2006). The “salience network”, including the insular cortex and anterior midcingulate cortex, has increased activity during emotion (e.g., Lindquist et al., 2012b), pain (e.g., Lamm et al., 2010), anxiety (e.g., Seeley et al., 2007), attention, language (see Nelson et al., 2010), and time perception (see Craig, 2009). Even sensory brain areas that were once thought to be unimodal and domain-specific (such as primary auditory and visual cortices) respond to other sensory domains (e.g., auditory neurons show increased activity during the presentation of visual stimuli; Bizley and King, 2008; visual neurons show increased activity during the presentation of auditory stimuli; Cate et al., 2009). These findings suggest that lack of support for faculty psychology is not merely an artifact of poor spatial or temporal resolution in neuroimaging techniques.
In fact, meta-analyses that summarize the neuroimaging literature on mental categories such as emotion, the self, memory, etc. confirm that brain regions show little psychological specificity (at least for these categories or for their subordinate categories such as anger, fear, disgust, the autobiographical self, self-referential processing, autobiographical memory, semantic memory, etc.). For instance, our meta-analytic project on emotion demonstrated that the amygdala (previously thought to be specifically related to fear), anterior insula (AI) (previously thought to be specifically related to disgust), anterior midcingulate cortex (aMCC) and orbitofrontal cortex (OFC) (previously thought to be specifically related to sadness and anger, respectively) each showed increased activity across the experience and perception of many different emotions, indicating that increased activity in these areas is not specific to any one emotion category (Lindquist et al., 2012b). Furthermore, during the experience and perception of emotion, there was increased activity in areas typically involved in autobiographical memory and prospection, language and semantics, and executive control (Barrett et al., 2007c, Kober et al., 2008, Lindquist et al., 2012b). Meta-analyses assessing the neural correlates of other mental states demonstrate a similar point. For instance, one meta-analysis found that the same set of midline cortical areas that comprise the “default network” (including the hippocampus, medial prefrontal cortex and posterior cingulate cortex) showed increased activity in memory, prospection for the future, theory of mind, spontaneous thought, and spatial navigation (Spreng et al., 2009). Another recent meta-analysis demonstrates that a similar set of regions within the dorsal prefrontal and parietal cortices is involved across working memory, response selection, response inhibition, task switching and cognitive control (Lenartowicz et al., 2010).
A second line of evidence supporting the viability of a constructionist approach to the mind comes from electrical stimulation and lesion studies. Electrical stimulation of the same site within the human brain produces different mental states across instances (Halgren et al., 1978, Sem-Jacobson, 1968, Valenstein, 1974). Even human lesion studies are consistent with the idea that brain regions are not specific to any one mental state. For instance, the speech disorder called Broca's aphasia is caused by lesions that extend beyond Broca's area, the brain region thought to subserve speech production (Mohr et al., 1978). As another example, amygdala lesions are not specifically associated with deficits in fear-related processing. A patient with bilateral amygdala lesions (i.e., SM) has difficulty perceiving fear on the faces of others (e.g., Adolphs et al., 1994, Adolphs et al., 1995, Adolphs et al., 1999), but more recent findings suggest that patient SM is capable of perceiving fear when her attention is explicitly directed to the eyes of a face (Adolphs et al., 2005) or when viewing caricatures of fearful body postures (Atkinson et al., 2007). These findings suggest that the amygdala might be playing a more general role in attention to novel or motivationally relevant stimuli that contribute to fear, but that the amygdala is not specific to fear (for discussions, see Cunningham and Brosch, 2012, Lindquist et al., 2012b).
Finally, the emerging science of “intrinsic networks” is consistent with the idea that the brain's functional architecture contains networks that correspond to domain-general psychological processes rather than to specific mental state categories. By correlating low-frequency blood-oxygenation level dependent (BOLD) signal fluctuations in the hemodynamic response of voxels when a brain is “at rest” (i.e., when it is not being probed by an external stimulus or engaging in a directed task), it is possible to identify large-scale distributed networks that span frontal, cingulate, parietal, temporal, and occipital cortices. These networks are highly replicable across studies that use different statistical methods and are observed with both seed-based (e.g., Vincent et al., 2008) and other multivariate techniques (e.g., independent component analysis; ICA; Smith et al., 2009) and cluster analysis (Yeo et al., 2011). These intrinsic networks are constrained by anatomical connections (Buckner, 2010, Deco et al., 2010, Fox and Raichle, 2007, Vincent et al., 2008), so they seem to reveal something about the functional organization that is fundamental to the human brain. Given that intrinsic activity accounts for a large proportion of the brain's metabolic budget (Raichle and Minton, 2006), it is possible that these networks might be basic psychological “ingredients” of the mind. Although a number of intrinsic networks have now been identified, none seem to map on to the brain activity that corresponds to the categories in a faculty psychology approach (i.e., there appears to be no one network for “anger” or even “emotion” vs. “cognition”).
In this paper, we report a novel study testing a constructionist model of the mind where we measured activity within large-scale distributed brain networks using fMRI as participants generated three kinds of mental states (emotions, body feelings, or thoughts). We then examined the similarity and differences in the pattern of network activity across the three mental states. In our experiment, participants were exposed to a new scenario immersion technique (Wilson-Mendenhall et al., 2011) that evokes mental events as they happen in everyday life, allowing us to study the sort of subjective experiences that are uniquely human (see also Frith, 2007). Psychology often assumes that mental states emerge only when a person is probed by external stimuli (based on an old model of the mind that was imported from physiology in the 19th century; Danziger, 1997). Yet, mental states do not obey this classic stimulus–response model most of the time—people do not need a stimulus in the physical world to have a rich and subjectively potent emotion, feeling, or thought (e.g., Killingsworth and Gilbert, 2010). We tried to do justice to this feature of mental life by using the scenario immersion technique as an ecologically valid method that directs mental content, while keeping some of the unrestrained character of subjective mental experience intact.
Participants heard sensory-rich, vivid, scenarios about unpleasant situations and were asked to create a situated conceptualization during which each situation was experienced as a body state (e.g., heartbeat, touch of an object against the skin, sights, smells, unpleasantness), an emotion (e.g., fear, anger) or a thought (e.g., plan, reflection). At the beginning of each trial, participants were cued to the type of mental state to construct on that trial. Following the cue, participants heard a scenario as they constructed and then elaborated on a body state, emotion, or thought. This imaging method was modeled after Addis et al. (2007) who asked participants to “construct” and then “elaborate” on autobiographical memories. We separately analyzed the scenario immersion and the construction + elaboration phases of each trial as two events (scenario immersion, experience).
Taking a network-based model of the mind as our starting assumption, we hypothesized that mental states were constructed from the interaction of networks (Fuster, 2006, Goldman-Rakic, 1988, McIntosh, 2000, Mesulam, 1998; also see Bullmore and Sporns, 2009), where the psychological function of a set of brain areas exists in the functional interaction of those areas. Specifically, we focused on the seven intrinsic networks recently identified by Yeo et al. (2011); these networks were derived from the largest sample of participants (N = 1000) in any study of intrinsic functional connectivity to date and also replicate the networks identified in other published reports (e.g., Fox et al., 2005, Seeley et al., 2007, Smith et al., 2009, Vincent et al., 2008). Table 1 lists the brain regions that are found to comprise each network across studies along with key papers that contribute to a functional understanding of each network.
We hypothesized that the so-called “limbic network” supports the brain's ability to generate and/or represent somatovisceral changes that are experienced as the core affective tone that is common to every mental state. Many philosophers and psychologists have proposed that every moment of mental life has some affective aspect (e.g., Wundt, 1897/1998) that can be described as a combination of hedonic pleasure and displeasure with some degree of arousal (Barrett and Bliss-Moreau, 2009, Russell and Barrett, 1999). In our constructionist view, we refer to this basic psychological element as “core affect” (Russell, 2003). Although the limbic network outlined by Yeo et al. (2011) is limited to a relatively small area of cortex (only covering the ventromedial prefrontal cortex and ventral aspects of the temporal cortex), several subcortical structures are also likely part of this limbic network. For instance, we hypothesize that the nuclei of the basal ganglia are part of a “limbic” network because they are involved in orchestrating effortful behavior (Salamone and Correa, 2002, Salamone et al., 2007) and motor control (Grillner et al., 2005). Furthermore, the central nucleus of the amygdala and the midbrain periaqueductal gray might be part of this network insofar that they are respectively involved in producing autonomic responses (for a discussion see Barrett et al., 2007c) and coordinating coherent physiological and behavioral responses (Bandler and Shipley, 1994, Van der Horst and Holstege, 1998). It is important to note that the basal ganglia, the amygdala, and the periaqueductal gray all project to the ventromedial prefrontal cortex (vmPFC), which is one of the cortical regions within Yeo et al.'s limbic network.
We hypothesize that the “salience network” (referred to as “ventral attention” by Yeo et al., 2011), uses representations of affect to guide attention and behavior (see Lindquist and Barrett, under review, Medford and Critchley, 2010). Importantly, the salience network contains aspects of the dorsal anterior insular cortex and anterior mid-cingulate cortex (aMCC), which are involved in executive attention (Corbetta et al., 2002, Touroutoglou et al., 2012) and interoception (Critchley et al., 2000, Critchley et al., 2004), suggesting that this network is an important source of affective attention in the human brain (Barrett and Bar, 2009, Duncan and Barrett, 2007). The salience network also contains aspects of the ventral anterior insula that is involved in the experience of affective states (Touroutoglou et al., 2012).
We hypothesize that the “default network” contributes to the representation or “simulation” of previous experience and the retrieval of category knowledge to create situated conceptualizations (i.e., to make meaning of somatovisceral changes in the body in relation to the immediate context). We hypothesize that this network is key to the process of reactivating relevant distributed brain regions to support category knowledge, memories, and prospection of the future by directing sensory and motor regions. Posterior aspects of the default network (e.g., posterior cingulate, precuneus, hippocampus) might be particularly involved in the integration of visuospatial aspects of category knowledge (Cavanna and Trimble, 2006) whereas anterior aspects of the default network (e.g., mPFC) might be involved in integration of the affective, social, and self-relevant aspects of category knowledge (Gusnard et al., 2001).
The “frontoparietal network” plays an executive role by modulating activity in other functional networks (i.e., prioritizing some information and inhibiting other information) to help construct an instance of a mental state. The “dorsal attention network” plays a similar role by directing attention, in particular, to visual information. We hypothesize that during the scenario immersion task, these networks contributed to the executive control processes involved in foregrounding certain types of information in conscious awareness to create one type of mental state over another. For example, although conceptualization is important to all states, it is particularly foregrounded in experiences of emotions and in thoughts. These networks ensure that a mental state is experienced as unified (for a discussion see Lindquist et al., 2012a).
Finally, “visual” and “somatomotor” networks are together involved in the representation of visual, proprioceptive, and auditory sensations. We refer to these as “exteroceptive” sensations because information from outside the body is represented as sounds, smells, tastes, proprioception, and sights. We assume that these sensations are important during the construction of all mental states.
Table 1 includes our hypotheses for each network's involvement in body feelings, emotions, and thoughts. First, we hypothesized that body feelings, emotions, and thoughts would involve some degree of affect, conceptualization, and executive attention (Hypothesis 1). Following this hypothesis, we predicted that the limbic network, the salience network, the default network, and the frontoparietal network would be commonly engaged across a conjunction of all mental states. Second, we hypothesized that a comparison of brain activity across mental states would yield relative differences in the contribution of each ingredient to each kind of state (Hypothesis 2). Specifically, we predicted that body states and emotions engage the limbic and salience networks relatively more than would thoughts (Hypothesis 2a) (see Table 1). We also predicted that thoughts and emotions would engage the default network relatively more than would body states, because we reasoned that conceptualization would play a larger role in mental states where the representation of prior experiences is necessary to make meaning of body sensations in the moment (i.e., emotion) or where representation of prior experiences is being used to guide plans, associations, and reflections about a situation (i.e., thought) (Hypothesis 2b) (see Table 1). Finally, we did not have a priori predictions for how the frontoparietal, dorsal attention, somatomotor, and visual networks would differ across the three classes of mental states.
Section snippets
Participants
Participants were twenty-one right-handed, native English-speaking adults (12 females, Mage = 26.42, SDage = 5.72). Participants gave written informed consent according to the Partners Health Care Institutional Review Board and were paid up to $200 for their participation. Potential participants indicated if they had a history of learning disabilities, psychiatric illness, claustrophobia, cognitive dysfunction or alcohol/drug abuse in a phone screening conducted prior to study enrollment.
Response time and subjective ratings
An analysis of the button press response times in seconds demonstrated a significant difference between mental states, F(2, 38) = 3.98, p < .05, η² = .17. Simple effects showed that participants constructed body feelings (M = 1.95, SD = 1.27) significantly more quickly than they constructed emotions (M = 2.61, SD = 1.28) and marginally more quickly than thoughts (M = 2.47, SD = 1.48). Yet, as expected, participants did not report differences in the ability to construct each type of state. Participants were
Discussion
To our knowledge, the present neuroimaging experiment is the first to explicitly test a constructionist functional architecture of the mind by assessing both similarities and relative differences in the neural correlates of body feelings, emotions, and thoughts. Our findings support the constructionist hypothesis that mental states are best understood by examining relative differences in the engagement of distributed networks that support psychological processes that are engaged to create a
Acknowledgments
Many thanks to Thomas Yeo, Fenna Krienen, and the Buckner lab for making the Yeo et al. (2011) network parcellation available. This research was supported by a National Institutes of Health Director's Pioneer award (DP1OD003312) to Lisa Feldman Barrett. The writing of this manuscript was supported by a Marie Curie International Outgoing Fellowship awarded by the Seventh Framework Program of the European Commission to Suzanne Oosterwijk and a Harvard University Mind/Brain/Behavior Postdoctoral
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Authors contributed equally.