Lindquist et al. are to be commended for meticulously integrating comprehensive reviews of basic emotion theory with detailed meta-analyses from the neuroimaging of emotion literature. Using the extant neuroimaging literature, they cogently argue that neuroimaging evidence does not support the locationist view that specific brain circuits underlie specific emotional experiences or perceptions. Although this conclusion is not necessarily the final word on the question, as acknowledged by the authors, given the early state of brain imaging technology, the target article makes a convincing case that alternative formulations of the neural basis of emotion and emotional experience are needed.

In general we agree with Lindquist et al. that a constructivist approach to emotional experience makes sense. Indeed, in 1987 one of us described a constructivist model of emotional experience driven by language (Lane & Schwartz Reference Lane and Schwartz1987). Where we disagree, however, is in the specific content of the constructivist model that is proposed. Throughout their article, Lindquist et al. assume that emotion must, at a minimum, be associated with the conscious experience or mental representation of emotion (“core affect”) that is valenced and associated with some degree of arousal. The authors also hold that further differentiation of experience results from linguistically determined categories of specific emotion that do not have any real existence in nature. While we agree that the differentiated experience of emotion is largely language-driven, our primary concern is that the nature of the process of the construction of emotional experience is, in our view, more complex than Lindquist et al. assert.

With the discovery that the vast majority of cognition does not occur consciously, and that each of the steps in the generation and unfolding of an emotional response involves information processing of some kind, one of us has argued that the distinction between implicit and explicit processes, a cornerstone of modern cognitive neuroscience, also applies to emotion (Lane & Nadel Reference Lane and Nadel2000). According to this perspective, the visceromotor and somatomotor manifestations of emotion may occur in the absence of emotional experience, and constitute implicit emotional responses.

There is now a considerable literature supporting this view. In a comprehensive review on emotional experience, Lambie and Marcel (Reference Lambie and Marcel2002) concluded that a two-level model of emotional experience is needed that can account for unconscious emotion, that is, emotional responses without conscious experience or awareness (see also Kihlstrom et al. Reference Kihlstrom, Mulvaney, Tobias, Tobis, Eich, Kihlstrom, Bower, Forgas and Niedenthal2000; Lane Reference Lane2008; LeDoux Reference LeDoux1996). Over the past 25 years or so, academic research has been conducted on implicit affect, that is, spontaneous affective reactions associated with changes in peripheral physiology and/or behavior that are not associated with conscious emotional experiences (cf. Quirin et al. Reference Quirin, Kazén and Kuhl2009a; Winkielman & Berridge Reference Winkielman and Berridge2004; Zajonc Reference Zajonc and Forgas2000). Lindquist et al. do not discuss the potential relevance of this distinction between implicit and explicit emotion processing for the analysis of neural correlates of emotion.

Furthermore, many decades of research preceding the modern era of neuroimaging demonstrated the evocation of visceral and somatomotor expressions of emotion in brainstem stimulation studies of laboratory animals (LeDoux Reference LeDoux1996). Although these phenomena cannot be scientifically linked to reportable experiences, they nevertheless are the bodily expression of emotion. We believe that implicit emotion, consisting of the visceromotor and somatomotor expressions of emotion, which may or may not be valenced, constitute the foundation upon which more differentiated emotional experience is built. Moreover, subcortical structures including the thalamus, hypothalamus, amygdala, and periaqueductal gray likely do contribute to the generation of undifferentiated emotional responses that are not associated with emotional experiences (Lane Reference Lane2008). Many brainstem structures are not well-visualized using modern imaging techniques, which may help to explain the under-emphasis of these phenomena by Lindquist et al.

According to this alternative perspective, the conscious experience of emotion (which could include core affect) requires communication between subcortical and cortical structures, both paralimbic (anterior cingulate, insula, orbitofrontal cortex) and neocortical (medial prefrontal cortex). During attentional awareness, when individuals explicitly focus on their affective reactions, the dorsal anterior cingulate cortex is active (see Phan et al. [Reference Phan, Wager, Taylor and Liberzon2004] for a meta-analysis), Furthermore, three different imaging studies have demonstrated that healthy individuals who are more emotionally aware engage the anterior cingulate cortex, particularly the dorsal portion, to a greater extent during emotional arousal (Frewen et al. Reference Frewen, Lane, Neufeld, Densmore, Stevens and Lanius2008; Lane et al. Reference Lane, Reiman, Axelrod, Yun, Holmes and Schwartz1998; McRae et al. Reference McRae, Reiman, Fort, Chen and Lane2008). In addition, reflective awareness of emotion involves the creation and integration of conceptual representations of emotional experiences that will affect the interpretation of future emotional experiences. Reflective awareness typically requires participation of structures in the paracingulate sulcus including the dorsomedial prefrontal cortex (Gusnard et al. Reference Gusnard, Akbudak, Shulman and Raichle2001; Lane et al. Reference Lane, Fink, Chau and Dolan1997; Ochsner et al. Reference Ochsner, Knierim, Ludlow, Hanelin, Ramachandran and Mackey2004a). These two levels of explicit processing are superimposed upon and integrated with implicit affective processes. In this sense, conscious emotional experiencing is a constructive process that integrates implicit and explicit affect.

We propose that the investigation of how elementary affective processes develop to become full-blown emotional experiences may provide additional insight into the degree to which emotions are constructed psychologically. In this context, relating implicit measures of emotion such as the Implicit Positive and Negative Affect Test (Quirin et al. Reference Quirin, Kazén and Kuhl2009a) to brain activity might be promising. Notably, the factor structure of this reliable indirect test divides into two types of implicit affect, positive and negative (see also Cacioppo et al. Reference Cacioppo, Gardner and Berntson1999; Gray & McNaughton Reference Gray and McNaughton2000; Watson et al. Reference Watson, Wiese, Vaidya and Tellegen1999), suggesting that valence becomes part of emotional responses prior to the construction of emotional experience (see Quirin et al. [Reference Quirin, Kazén, Rohrmann and Kuhl2009b] for relationships of implicit but not explicit affect with cortisol; also see Zajonc Reference Zajonc and Forgas2000). Furthermore, the neural correlates of emotional responses can be investigated as a function of individual differences in emotional awareness (Lane et al. Reference Lane, Quinlan, Schwartz and Walker1990). Such approaches may contribute to the disentangling of the functional components of emotion, including somatic processes (peripheral physiological arousal and action tendencies), specific emotional experiences of a single type, blends of emotional experience, as well as regulation processes, all of which are typically implicated in affective responses and their neural correlates.