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Demythologizing the emotions: Adaptation, cognition, and visceral representations of emotion in the nervous system
Brain and Cognition 52 (2003) 15–23 www.elsevier.com/locate/b&c
Demythologizing the emotions: Adaptation, cognition, and visceral representations of emotion in the nervous system Jay Schulkin,a,* Barbara L. Thompson,b and Jeffrey B. Rosenb a
Department of Physiology and Biophysics, School of Medicine, Georgetown University, Washington DC, 20007, USA b Department of Psychology, University of Delaware, Newark, DE 19716, USA Accepted 26 September 2002
Abstract This article highlights four issues about the neurobiology of emotions: adaptation vs. dysfunction, peripheral and central representations of emotion, the regulation of the internal milieu, and whether emotions are cognitive. It is argued that the emotions evolved to play diverse adaptive roles and are biologically vital sources of information processing. They were not designed as pieces of pathology, though they certainly can underlie some psychophathologies. Emotions are, in part, appraisal systems that are operative at numerous level of the nervous system from the brainstem to the cortex. Like other information processing systems they are not perfect cognitive systems. Emotional systems often utilize somatic and visceral information for appraisals of events to facilitate decisions of whether to approach or avoid objects. The neural systems of emotions traverse the entire neural axis and are linked to the regulation of the internal milieu. Thus, in addition to the experiential aspects of emotions, emotions embody appraisal systems that are pervasive to all levels of the brain to facilitate function, adaptation, and survival. Ó 2003 Elsevier Science (USA). All rights reserved.
1. Introduction and historical context There is a long history of casting a disparaging intellectual gaze at the emotions. A tradition that dates back to Plato (1956) and continues through Freud (1924/1960) and still resonates today, understands the emotions as rendering one vulnerable to thoughtlessness. The emotions were conceived as powerful, but also brute, disorganizing and stuporous (Sartre, 1948). This conception has had a stranglehold over our sense of who we are with regard to this very important part of ourselves. It has led many an investigator to leave emotion out of their sphere of inquiry, since they were viewed as mostly noise. A dominant, rationalist tradition elevated the cogito (e.g., Spinoza) and castigated the emotions. According to this tradition, emotions render one passive (e.g., Spinoza, 1668/1955). As one classical rationalist stated the issue ‘‘by emotion I mean modification of the body. . .’’ and is a ‘‘confused idea’’ (Spinoza, 1668/1955). Passivity was linked to the emotions; the cogito was * Corresponding author. Fax: 1-202-863-4994. E-mail address: [email protected] (J. Schulkin).
linked to self-determination. This misguided conception held sway for centuries, and many investigators still reflexively follow this conception (Sartre, 1948). When the cognitive sciences emerged in the late 20th century as a legitimate scientific enterprise following the demise of the narrow-minded behavioristic tradition, it made the similar mistake that behaviorism made of discounting or downplaying biology and the emotions. The emotions were seen as ‘‘secretory’’ (Rey, 1980), bodily and less than rational. The cognitive revolution was obsessed with abstract rules, rules that guided behavior, multiple codes for internal representations (Fodor, 1983; Posner, 1990; Rey, 1997; Von Eckert, 1993). Representations and their structures were the guiding framework of the cognitive sciences. However, it became apparent that abstract rules are not the only psychological events to account for everyday reasoning—rough and ready heuristics play a major part, where everyday practice is replete with good enough problem-solving (Baron, 1990; Gigerenzer, 1991; Khaneman, Slovic, & Tversky, 1982; Simon, 1956, 1979, 1982). Emotions are part of this rough and ready paradigm and are important problem-solving tools in the armament of adaptation. Emotional information processing can be
0278-2626/03/$ - see front matter Ó 2003 Elsevier Science (USA). All rights reserved. doi:10.1016/S0278-2626(03)00004-6
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competent, like other forms of reasoning, and can be fast and accurate or inaccurate, with an imperfect knowledge base. This reminds one of good enough parenting; there is certainly no perfect parenting. This is where the emotions have a place in problem-solving, as good and sometimes elegant, but imperfect tools for survival. A large number of cognitive scientists have now begun to accept the reality of the emotions (Gazzaniga, 1995/2000; Lane & Nadel, 1999). Unfortunately, it still appears that they are often still characterized pejoratively. Some investigators distinguish emotions from ‘‘real solid’’ problem-solving (Lowenstein, 1996), or worse, associate emotional expression with pathology. But pathology afflicts many functional systems in the brain that can be dissociated from emotional information systems, particularly those of movement and memory disorders (e.g., HuntingtonÕs and AlzheimerÕs). These pathologies are rooted in functional systems of motor control and memory, just as anxiety disorders are rooted in functional systems of adaptive fear behavior (Davis & Whalen, 2001; Rosen & Schulkin, 1998). With the acceptance of the reality of emotions has come intense debate about the functions of the emotions. We would like to briefly address a number of topics in emotion research. One topic is whether emotions are adaptive or dysfunctional; a second is whether the periphery and viscera are integral parts of emotion; a third is how these parts interact with regulation of the internal milieu: hedonic central experiences. A fourth is whether emotional processing is cognitive or non-cognitive. In our brief discussion a recurrent theme through each section is about demythologizing the emotions (i.e., emotional systems are neither perfect nor flawed) and placing them within a biological context, one in which the emotions are a vital piece of our information processing systems.
2. Emotions and adaptation Those influenced early by biology, and specifically by Darwin (1872/1965), envisioned the emotions in functional adaptive terms; this is particularly true in the work of William James (1884, 1890/1952) and John Dewey (1895). Emotions were part of how one orients to a problem, the processing of information and the resolution of a problematic context. Importantly, emotions were not understood as simple sensory pulls and pushes. Animals came evolutionarily prepared to emit signals to others and to understand them; they came prepared to appraise events for their significance. Emotions are part of the information processing systems of a wide variety of animals (see Fig. 1). In an adaptationist view, the emotions are not passive and pejorative states, and should not be viewed exclusively in a negative light. Although environmental
Fig. 1. A cat in a familiar position (Darwin, 1872/1965). This is a reflexive response rich in bodily sensibility and information processing.
pressures during much of animal and human evolution are very different than our present day pressures, emotional responses and behaviors were selected by evolutionary forces as part of successful adaptation. Indeed, it appears that emotional information is critical for appropriate personal and social decisions. Whether information processing is construed in historical terms as cognitive or emotional is not the question. What is important to understand is the myriad of ways in which animals are prepared to emit signals, process information and solve problems (Hauser, 2000; Marler, 2000). Emotions, at times, can be elegant forms of problemsolving. At other times they can be fallible. All reasoning labors under the constraints of fallibility. There is nothing here to rarify, reify, or denigrate about the emotions and their role in problem-solving. Emotional appraisals can be fast (Todd & Gigerenzer, 2000) or slow and lexically rich, but fallible. Once the mythology of ‘‘perfect reason’’ is eradicated from the pantheon of human expression and understanding, surely the emotions can be established as legitimate forms of problemsolving. Emotions are about action, or at least action tendencies (Frijda, 1986). At a minimum the purpose of emotions is to produce specific physiological and behavioral responses to stimuli that prepare an animal to move toward or away from animate and inanimate objects (Davidson, Ekman, Saron, & Semios, 1990; Schnierla, 1966). These stimulus–emotional response relationships have been sculpted by evolution and have an adaptive logic—reason that is grounded in the biological history of each species (Pinker, 1997; Rozin, 1998).
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We do not want to overstate the case that emotions are axiomatically adaptive; they are not. But let us not denigrate emotion into something that renders us less able to understand or generate adaptive behavior to cope with our surroundings. Emotions may be less than perfect, but no less essential than other forms of information processing. We want to know how the emotions can be adaptive and where the emotions breakdown and become dysfunctional.
3. Peripheral and central representations of emotion A debate that began during the birth of academic psychology in the late 19th and early 20th centuries is whether the periphery and viscera are central to the emotions (e.g., Bard, 1928; Cannon & Britton, 1927; James, 1884). While this debate is still with us, bodily information is obviously fundamental in the organization of behavior, emotional, or otherwise (e.g., Adolphs, Damasio, Tranel, Cooper, & Damasio, 2000; Damasio, 1996; Ekman & Davidson, 1994; Panksepp, 1998; Rolls, 1999; Stellar, 1954, 1974). In our view, the use of central, peripheral, and visceral information is what distinguishes emotion from nonemotional cognition. In other words, the viscera is used in emotional information processing. Peripheral autonomic, visceral and somatic inputs inform decisionmaking about external objects and internal needs. Data, for example, showing that lesions of the ventro-medial prefrontal cortex impair both peripheral autonomic nervous system responses and advantageous decisions in both social and financial situations are recent examples that emotional information processing are part of problem-solving and decision-making (Bechara, Damasio, & Damasio, 2000; Dolan, 2000; Lane & Nadel, 1999). In other words, numerous, diverse demonstrations illustrate that autonomic input is compromised in frontal patients (Bechara et al., 2000), and therefore their decision-making is compromised, or conversely autonomic/visceral input is utilized in normal function (Damasio, 1996; Dolan, 2000; Rolls, 2000). Bodily contribution does not obviously mean bodily infallibility. This integration of peripheral and central nervous systems is reflected in the anatomical revolution of the 1970s and 1980s in which an explosion of knowledge changed our understanding of the structure and circuitry of the mammalian nervous system. For instance, in the late 1960s seven pathways to and from the amygdala were known (Larry Swanson, personal communication, 2001). Today there are nearly 700 amygdala input and outputs (Aggleton, 1992/2000; Nauta & Feirtag, 1986; Swanson, 1992, 1999). Other findings demonstrated brainstem visceral projections to the cortex, and direct projections from the neo- and pallocortex to brainstem sites have direct control of viscera function (Norgren,
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1995; Saper, 1996; Swanson, 1992). Visceral information from the heart and gastrointestinal organs can reach the amygdala and insular cortex within one or two synapses from the solitary and parabrachial nuclei of the brainstem (Allen, Saper, Hurley, & Cechetto, 1991; Saper, 1982). Our notion of the limbic system (Broca, 1878; MacLean, 1949; Papez, 1937) has also continued to evolve to the point where a unitary limbic system for emotion is questioned for its validity (Herbert & Schulkin, 2002; LeDoux, 1996; Saper, 1996; Swanson, 2000). There is, however, a visceral neural axis. In both chemical and functional terms the visceral nervous system information traverses all levels of the nervous system, from regions of the solitary tract and parabrahical nuclei to the amygdala and bed nucleus of the stria terminalis and regions of the neocortex (Allen et al., 1991; Norgren, 1995; Saper, 1996; Swanson, 2000). In contrast to a unitary emotional system, there are likely numerous circuits for different types of emotions (Calder, Lawrence, & Young, 2001; Ekman & Davidson, 1994; Lane & Nadel, 1999). Some circuits may be parallel (e.g., fear and joy), while others more integrated for particular emotions (e.g., fear and anger). These circuits are likely not segregated but use bits and pieces of circuits of one emotion for circuitry of other emotions. For example, the circuitry of the amygdala is an integral component of many types of fear, but may also be used to modulate anger-like behavior that may primarily be a function of other circuits (Calder et al., 2001; Rosen & Schulkin, 1998) e.g., septum-hypothalamus (Gray, 1982). The amygdala is also importantly linked to a number of functions other than fear (Emery et al., 2001; Gallagher & Holland, 1994; Davis & Whalen, 2001; Schulkin, 1991, 1999: social appraisals, reward, attention, appetite). Similarly, neural circuits involved in emotions may also subserve other functions. The amygdala is a major component of taste/visceral connectivity to the brainstem and these visceral pathways underlie motivated behavior (Herrick, 1905; Norgren, 1995; Pfaffmann, Norgen, & Grill, 1977; Spector, 2000). Importantly, many of the neuropeptides that play a key role in the organization and expression of adaptive responses are found along the gustatory–visceral axes. Neuropeptides, for example, such as angiotensin and corticotropin releasing hormone (CRH) or oxytocin are found in many of the sites along the taste/visceral pathways (Gray, 1999; Lind, Swanson, & Ganten, 1984; Swanson, 1992). The chemical pathways also play vital roles in the organization of emotions and they are represented in both the peripheral and central nervous systems (see Fig. 2). While all neurotransmitters play a role in the organization of central states, we want to use the neuropeptides as illustrative examples of how the peripheral
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Fig. 2. The three drawings from top to bottom: corticotropin releasing hormone (CRH) in the brain (Swanson, Sawchenko, Rivier, & Vale, 1983), angiotensin sites in the brain (Lind et al., 1984), and the central gustatory neural axis (Norgren, 1995). The point one should note is that many of the peptide sites overlap with gustatory–visceral sites in the brain.
Fig. 3. Repeated systemic administered corticosterone (CORT) given before training enhances long-term memory for contextual fear conditioning. The mean SEM percent time spent freezing was measured immediately after the training (post-shock) or in a retention test 24 h after conditioning (retention). There were no differences in post-shock freezing, while freezing in the retention test was significantly facilitated by repeated CORT (shown in the figure). The * denotes that in the Vehicle group freezing during the retention test was significantly different from post-shock freezing. (Digitized images of corticotropin releasing hormone (CRH) mRNA in the central nucleus of the amygdala (CeA; arrows) 2 h after the last of twice daily VEHICLE or CORT injections for 5 days.) CRH mRNA in the CeA was significantly increased by repeated CORT administration (p < :02). One mechanism to increase vigilance, attention and memory is the upregulation by CORT on CRH neurons within the visceral neural axis that are organizing the behavioral responses associated with fear (Thompson et al., 2000).
and central systems can use the same endogenous chemicals. Nature is opportunistic to use the same sets of molecules to subserve systemic physiologic representation and central organization of behavior. For example, oxytocin in the septum and bed nucleus of the stria terminalis is linked to attachment behaviors; in the periphery they are involved in milk letdown and lactation (Carter, 1998; Insel, 1992). The central expression of oxytocin, as a neuropeptide, is linked to decisions to approach or avoid objects and is mediated by regions of the brain which may include the amygdala, bed nucleus of the stria terminalis and no doubt influencing regions of the frontal cortex (Carter, Lederhendler, & Kirkpatrick, 1997/1999; Insel, 1992). Attachment behavior is a fundamental way in which children and many other kinds of animals (Bowlby, 1988; Hofer & Sullivan, 2001; Tinbergen, 1951) get oriented to the world and find security. The appraisal mechanisms may often be reflexive and fast (Oatley & Jenkins, 1996), but with age and experience perhaps less so. The states of fear and alertness to external events have been linked to extra-hypothalamic expression of the neuropeptide CRH, particularly in the central nucleus of the amygdala and the bed nucleus of the stria
terminalis (e.g., Gray, 1999; Lee & Davis, 1997; Schulkin, 1999). Along the visceral neural axis is information related to autonomic and behavioral adaptation and CRH expression is linked to appraisal of events that are linked to danger, or novelty (Davis & Whalen, 2001; Habib et al., 2000; Kalin, Shelton, & Davidson, 2000; Rosen & Schulkin, 1998). The expression of CRH is also linked to frontal neocortical activation (Kalin et al., 2000). Importantly, input from peripheral sites, such as the adrenal gland (and the production of cortisol or corticosterone), acts to facilitate neuropeptide expression CRH. One result is to facilitate a central state of fear (Corodimas, LeDoux, Gold, & Schulkin, 1994; Thompson, Schulkin, & Rosen, 2000) (see Fig. 3). Another neuropeptide, that underlies visceral expression and that is fundamental in generating a behavior, is angiotensin. Angiotensin is essential for thirst and sodium intake, including the central state of search, recalling past associations and feeling satisfied when ingesting water or sodium (Denton, McKinley, & Weisinger, 1996; Fitzsimmons, 1999). Angiotensin plays diverse roles in the periphery essential for maintaining body fluid balance, while in the brain it is essential for organizing behavioral responses. Thus, angiotensin
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expression in the brain is important for palatability and affective appraisals for body fluid regulation. There is nothing abstract and divorced about the representation of fluid balance at a number of levels within the visceral neural axis (Fitzsimmons, 1999; Herbert & Schulkin, 2002). Each of these neuropeptides serves both physiological and behavioral regulation. They are information molecules (Herbert & Schulkin, 2002; see also Berridge & Robinson, 1998 and Schultz, Tremblay, & Hollerman, 2000 for a discussion of a neurotransmitter) in the visceral nervous system that are essential for behavioral viability. These three examples, and there are a number of others (Carter et al., 1997/1999; Schulkin, 1999), contribute importantly to both peripheral autonomic and central representations in the organization and expression of the emotions.
4. Emotions and the regulation of the internal milieu: Hedonic experiences Adherents of the tradition of regulatory physiology understood that behavior is vital to sustain internal homeostatic balance and adaptations to perturbation (Richter, 1976). Central states of the brain, informed by visceral representations, guide behavioral responses (Stellar, 1974). These are not divorced abstract representations that discard the body, but the body informs the brain allowing it to respond appropriately (Denton et al., 1996). Alterations in homeostatic balance and internal physiology impact the brain to generate behaviors, to ameliorate discomforts, and so forth. Brains of many animal species have evolved to a point where neural information processing systems are designed to not only respond to internal changes but to anticipate them. Along with anticipation, the intensity of internal stimulation, and the memory of the intensity, is a fundamental trigger in approach or avoidance mechanisms (Schnierla, 1966). Judgements to approach or avoid reflect the activation of the brain circuits throughout the neural axis. Circuits involving the frontal cortex (e.g., Davidson et al., 1990; Schmidt & Fox, 1999), the striatum (Calder et al., 2001; Saper, 1996; Schultz et al., 2000), amygdala and hypothalamus (LeDoux, 1996; Saper, 1996; Stellar & Stellar, 1985; Swanson, 2000) and brainstem regions, to give a few examples, are all essential for carrying out the full range of behavioral responses. A wide variety of objects (foods, people, and settings), either learned or not learned, are powerful elicitors of approach behaviors. These approach behaviors are importantly linked to palatability judgements and appraisal mechanisms (i.e., what something looks like, what it tastes like, if it is sweet, if the texture is soft, if the body is inviting). We would suggest that preferences
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Fig. 4. Gluttonous pleasurable experience, and unfortunately associated with the lack of control and the expression of the emotions.
do in fact need inferences (cf. Lazarus, 1991; Sabini & Silver, 1998; Zajonc, 1980, 2000), they are just low-level appraisal systems (discussed in following section). Hedonic experiences linked to palatability judgements are also important features that motivate behavior (e.g., Berridge, 1996, 2000; Pfaffmann et al., 1977; Stellar, 1974). A question is whether emotional and hedonic experiences are the same or not. Both inform, both motivate and organize behavior. Nevertheless, hedonic experiences are not identical with emotions. For example, love (an emotion) is not an orgasm, but orgasms are awfully motivating (see Fig. 4). It has also been suggested (Sabini & Silver, 1998) that motivation should replace emotions in our scientific lexicon. In this view, motivation (the search for sodium, avoidance of fear-related events, etc) is adaptive, but emotions are not (see also Sartre, 1948). In a more integrated adaptive-functional view, motivations are also mechanisms for survival and are related to emotions, but distinct from emotions. What is important to note is that some rich traditions did not commit ‘‘DescartesÕ Error’’ (Damasio, 1994) of dissociating cognition from bodily experience. Those concerned with information processing within physiological systems essential for homeostatic (e.g., body temperature, fluid balance) and non-homeostatic (e.g., defensive) functions did not detach the impact of bodily experience from real world decisions (Garcia, Hankins, & Rusiniak, 1974; Richter, 1976; Stellar, 1974). Some of the circuits for emotional expression are also utilized in the organization of behaviors important for maintaining homeostatic and non-homeostatic systems.
5. Is emotional processing cognitive or non-cognitive? There is a well-known controversy about whether the emotions are cognitive or pre-cognitive processing. We believe emotional processing is cognitive. This does not mean that emotions are necessarily conscious or the cognitive processes are transparent to the individual. Just as neural processing and machinations of other cognition systems are unconscious, so are those of emotions. Appraisal occurs in all emotional responses (Ekman, 1992; Pinker, 1997). Appraisals, either nonemotional or emotional, can be fast and automatic such
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as the recognition of syntax, or the recognition of a happy or sad face (Young, 1998). The fact that the appraisal of both types of stimuli can be fast suggests that the mechanisms of information processing are evolutionary prepared to respond to certain sorts of stimuli, and that certain kinds of prepared learning and associations are intrinsic to problem-solving (Rozin, 1998). Fast- or slow-acting systems designed to enhance problem-solving are not perfect systems, and do not need to be perfect in order to be legitimate and selected by evolution (Gigerenzer, 1991; Simon, 1979, 1982; Todd & Gigerenzer, 2000). Emotions are no less cognitive aids than other forms of problem-solving. However, what makes emotions special is the intimate relationship of appraisal mechanisms and response or output systems. Brain mechanisms of appraisal and response of a particular emotion are parts of an integrated circuitry. For example, with the emotion of fear, appraisal mechanisms are partially embodied in the lateral and basal nuclei of the amygdala and output is initiated in the adjacent central nucleus of the amygdala (LeDoux, 1996, 2000; Swanson & Petrovich, 1998). Connections from the appraisal mechanisms directly project to the output pathways. In other words, with appraisal mechanisms so intimately tied to emotional output/behavioral responses it would be very difficult to evaluate an emotionally provoking stimulus without having a tendency to act or produce an actual overt response. Importantly, this is different from nonemotional cognitive processing like language, where input processing (WernickeÕs area) is connected but not adjacent or intimately integrated with the motor output of language (BrocaÕs area) and can be dissociated by lesions or brain damage. Automatic and evolutionarily conserved emotional appraisal may be exemplified by recent studies demonstrating that predator odors elicit fear-like responses in rats that have never experienced these odors before (Dulac, 2000; Wallace & Rosen, 2001). The first time rats are presented with an odorant isolated from fox feces they display avoidance and fear-like behavior, suggesting that laboratory rats have unconditioned fear to predator odor. Furthermore, lesions of the amygdala that impair learning of conditioned fear as measured by freezing behavior have little effect on unconditioned freezing to the predator odorant (Wallace & Rosen, 2001). The effects of amygdala lesions cannot be at the level of behavioral output because freezing to the predator odor was robust in amygdala-lesioned rats. The amygdala lesion likely disrupted appraisal and learning and memory mechanisms for conditioned fear. Thus, while learned fear may need the amygdala for appraisal of conditioned fear stimuli, appraisal of unconditioned fear of predator odor may occur at other levels of brain (Fendt, Endres, & Apfeobach, 2003), possibly even as early as the sensory mechanisms for olfaction.
Does the fast, automatic and possibly innate processes of emotions denigrate them? Does it make them less cognitive than deliberate thought? We think not. Cognition should not be viewed narrowly as conscious information processing, but as processing that can have multiple levels from simple habituation and sensitization to willful, conscious, decision-making. Moreover, we are not denying the experience of the emotions, in fact, the experience is part of the transaction with the environment (Dewey, 1925/1989; Schulkin, 2000), the experience of fear, joy, delight, etc. To say that the emotions are part of the biological mechanisms of information processing systems is not to denigrate them or leave the experience out of the explanation. It makes emotions ripe for scientific inquiry at multiple levels of analysis.
6. Conclusion Advances in the behavioral/cognitive and neural sciences have expanded our understanding of the mechanisms and functions of the emotions. The emotions are vital for information processing of many stimuli and experiences. There certainly are differences in the brain related to different kinds of information processing in cortical and sub-cortical areas involved in emotions and other kinds of events (Bush, Luu, & Posner, 2000; Calder et al., 2001; Davidson, Putnam, & Larson, 2000; Dolan, 2000; Price, Carmichael, & Drevets, 1996). We have emphasized that the viscera and numerous levels of the neural axis are involved in information processing subserving different and overlapping functions with regard to the emotions. For example, the amygdala and the prefrontal cortex subserve different functions in the appraisal and analysis of fear-related stimuli (Bechara et al., 2000; Calder et al., 2001; Wright et al., 2000). And importantly, the amygdala may be activated when one looks at something fearful, imagines something fearful, or reads a sentence about something fearful. While the experience of feeling is intrinsic to human emotions, we prefer the language of diverse appraisal systems (Dewey, 1925/1989; Goldman, 1986; Lazarus, 1991) when describing the emotions, as opposed to feelings that are distinct from cognition. The debates about separating feeling from cognition are endless, and perhaps not fruitful. Affective computational systems or appraisal–response systems would seem a good way to describe emotional processing and promote empirical study on emotions. Appraisal mechanisms are pervasive to systems of both approach and avoidance, and are thus parts of emotions, motivations, and central states. Appraisals may be low level, and certainly unconscious in terms of mechanisms of action. Moreover, appraisal systems do not sit at one level of the brain (cortex) and pure reception at another (brainstem); filter systems, encoding
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systems receptor fields, are pervasive throughout the nervous systems. The language of appraisal should not be rarified in cortical space; it exists in the lower brainstem (e.g., solitary and parabrachial nuclei). But to say that the emotions are informational systems is not to say that this is all they are. And we hope that by continually demythologizing the emotions they do not become either elevated or denigrated, but our understanding and appreciation of these very important aspects of life that were favored during our evolutionary development are enhanced.
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Demythologizing the emotions: Adaptation, cognition, and visceral representations of emotion in the nervous system Jay Schulkin,a,* Barbara L. Thompson,b and Jeffrey B. Rosenb a
Department of Physiology and Biophysics, School of Medicine, Georgetown University, Washington DC, 20007, USA b Department of Psychology, University of Delaware, Newark, DE 19716, USA Accepted 26 September 2002
Abstract This article highlights four issues about the neurobiology of emotions: adaptation vs. dysfunction, peripheral and central representations of emotion, the regulation of the internal milieu, and whether emotions are cognitive. It is argued that the emotions evolved to play diverse adaptive roles and are biologically vital sources of information processing. They were not designed as pieces of pathology, though they certainly can underlie some psychophathologies. Emotions are, in part, appraisal systems that are operative at numerous level of the nervous system from the brainstem to the cortex. Like other information processing systems they are not perfect cognitive systems. Emotional systems often utilize somatic and visceral information for appraisals of events to facilitate decisions of whether to approach or avoid objects. The neural systems of emotions traverse the entire neural axis and are linked to the regulation of the internal milieu. Thus, in addition to the experiential aspects of emotions, emotions embody appraisal systems that are pervasive to all levels of the brain to facilitate function, adaptation, and survival. Ó 2003 Elsevier Science (USA). All rights reserved.
1. Introduction and historical context There is a long history of casting a disparaging intellectual gaze at the emotions. A tradition that dates back to Plato (1956) and continues through Freud (1924/1960) and still resonates today, understands the emotions as rendering one vulnerable to thoughtlessness. The emotions were conceived as powerful, but also brute, disorganizing and stuporous (Sartre, 1948). This conception has had a stranglehold over our sense of who we are with regard to this very important part of ourselves. It has led many an investigator to leave emotion out of their sphere of inquiry, since they were viewed as mostly noise. A dominant, rationalist tradition elevated the cogito (e.g., Spinoza) and castigated the emotions. According to this tradition, emotions render one passive (e.g., Spinoza, 1668/1955). As one classical rationalist stated the issue ‘‘by emotion I mean modification of the body. . .’’ and is a ‘‘confused idea’’ (Spinoza, 1668/1955). Passivity was linked to the emotions; the cogito was * Corresponding author. Fax: 1-202-863-4994. E-mail address: [email protected] (J. Schulkin).
linked to self-determination. This misguided conception held sway for centuries, and many investigators still reflexively follow this conception (Sartre, 1948). When the cognitive sciences emerged in the late 20th century as a legitimate scientific enterprise following the demise of the narrow-minded behavioristic tradition, it made the similar mistake that behaviorism made of discounting or downplaying biology and the emotions. The emotions were seen as ‘‘secretory’’ (Rey, 1980), bodily and less than rational. The cognitive revolution was obsessed with abstract rules, rules that guided behavior, multiple codes for internal representations (Fodor, 1983; Posner, 1990; Rey, 1997; Von Eckert, 1993). Representations and their structures were the guiding framework of the cognitive sciences. However, it became apparent that abstract rules are not the only psychological events to account for everyday reasoning—rough and ready heuristics play a major part, where everyday practice is replete with good enough problem-solving (Baron, 1990; Gigerenzer, 1991; Khaneman, Slovic, & Tversky, 1982; Simon, 1956, 1979, 1982). Emotions are part of this rough and ready paradigm and are important problem-solving tools in the armament of adaptation. Emotional information processing can be
0278-2626/03/$ - see front matter Ó 2003 Elsevier Science (USA). All rights reserved. doi:10.1016/S0278-2626(03)00004-6
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competent, like other forms of reasoning, and can be fast and accurate or inaccurate, with an imperfect knowledge base. This reminds one of good enough parenting; there is certainly no perfect parenting. This is where the emotions have a place in problem-solving, as good and sometimes elegant, but imperfect tools for survival. A large number of cognitive scientists have now begun to accept the reality of the emotions (Gazzaniga, 1995/2000; Lane & Nadel, 1999). Unfortunately, it still appears that they are often still characterized pejoratively. Some investigators distinguish emotions from ‘‘real solid’’ problem-solving (Lowenstein, 1996), or worse, associate emotional expression with pathology. But pathology afflicts many functional systems in the brain that can be dissociated from emotional information systems, particularly those of movement and memory disorders (e.g., HuntingtonÕs and AlzheimerÕs). These pathologies are rooted in functional systems of motor control and memory, just as anxiety disorders are rooted in functional systems of adaptive fear behavior (Davis & Whalen, 2001; Rosen & Schulkin, 1998). With the acceptance of the reality of emotions has come intense debate about the functions of the emotions. We would like to briefly address a number of topics in emotion research. One topic is whether emotions are adaptive or dysfunctional; a second is whether the periphery and viscera are integral parts of emotion; a third is how these parts interact with regulation of the internal milieu: hedonic central experiences. A fourth is whether emotional processing is cognitive or non-cognitive. In our brief discussion a recurrent theme through each section is about demythologizing the emotions (i.e., emotional systems are neither perfect nor flawed) and placing them within a biological context, one in which the emotions are a vital piece of our information processing systems.
2. Emotions and adaptation Those influenced early by biology, and specifically by Darwin (1872/1965), envisioned the emotions in functional adaptive terms; this is particularly true in the work of William James (1884, 1890/1952) and John Dewey (1895). Emotions were part of how one orients to a problem, the processing of information and the resolution of a problematic context. Importantly, emotions were not understood as simple sensory pulls and pushes. Animals came evolutionarily prepared to emit signals to others and to understand them; they came prepared to appraise events for their significance. Emotions are part of the information processing systems of a wide variety of animals (see Fig. 1). In an adaptationist view, the emotions are not passive and pejorative states, and should not be viewed exclusively in a negative light. Although environmental
Fig. 1. A cat in a familiar position (Darwin, 1872/1965). This is a reflexive response rich in bodily sensibility and information processing.
pressures during much of animal and human evolution are very different than our present day pressures, emotional responses and behaviors were selected by evolutionary forces as part of successful adaptation. Indeed, it appears that emotional information is critical for appropriate personal and social decisions. Whether information processing is construed in historical terms as cognitive or emotional is not the question. What is important to understand is the myriad of ways in which animals are prepared to emit signals, process information and solve problems (Hauser, 2000; Marler, 2000). Emotions, at times, can be elegant forms of problemsolving. At other times they can be fallible. All reasoning labors under the constraints of fallibility. There is nothing here to rarify, reify, or denigrate about the emotions and their role in problem-solving. Emotional appraisals can be fast (Todd & Gigerenzer, 2000) or slow and lexically rich, but fallible. Once the mythology of ‘‘perfect reason’’ is eradicated from the pantheon of human expression and understanding, surely the emotions can be established as legitimate forms of problemsolving. Emotions are about action, or at least action tendencies (Frijda, 1986). At a minimum the purpose of emotions is to produce specific physiological and behavioral responses to stimuli that prepare an animal to move toward or away from animate and inanimate objects (Davidson, Ekman, Saron, & Semios, 1990; Schnierla, 1966). These stimulus–emotional response relationships have been sculpted by evolution and have an adaptive logic—reason that is grounded in the biological history of each species (Pinker, 1997; Rozin, 1998).
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We do not want to overstate the case that emotions are axiomatically adaptive; they are not. But let us not denigrate emotion into something that renders us less able to understand or generate adaptive behavior to cope with our surroundings. Emotions may be less than perfect, but no less essential than other forms of information processing. We want to know how the emotions can be adaptive and where the emotions breakdown and become dysfunctional.
3. Peripheral and central representations of emotion A debate that began during the birth of academic psychology in the late 19th and early 20th centuries is whether the periphery and viscera are central to the emotions (e.g., Bard, 1928; Cannon & Britton, 1927; James, 1884). While this debate is still with us, bodily information is obviously fundamental in the organization of behavior, emotional, or otherwise (e.g., Adolphs, Damasio, Tranel, Cooper, & Damasio, 2000; Damasio, 1996; Ekman & Davidson, 1994; Panksepp, 1998; Rolls, 1999; Stellar, 1954, 1974). In our view, the use of central, peripheral, and visceral information is what distinguishes emotion from nonemotional cognition. In other words, the viscera is used in emotional information processing. Peripheral autonomic, visceral and somatic inputs inform decisionmaking about external objects and internal needs. Data, for example, showing that lesions of the ventro-medial prefrontal cortex impair both peripheral autonomic nervous system responses and advantageous decisions in both social and financial situations are recent examples that emotional information processing are part of problem-solving and decision-making (Bechara, Damasio, & Damasio, 2000; Dolan, 2000; Lane & Nadel, 1999). In other words, numerous, diverse demonstrations illustrate that autonomic input is compromised in frontal patients (Bechara et al., 2000), and therefore their decision-making is compromised, or conversely autonomic/visceral input is utilized in normal function (Damasio, 1996; Dolan, 2000; Rolls, 2000). Bodily contribution does not obviously mean bodily infallibility. This integration of peripheral and central nervous systems is reflected in the anatomical revolution of the 1970s and 1980s in which an explosion of knowledge changed our understanding of the structure and circuitry of the mammalian nervous system. For instance, in the late 1960s seven pathways to and from the amygdala were known (Larry Swanson, personal communication, 2001). Today there are nearly 700 amygdala input and outputs (Aggleton, 1992/2000; Nauta & Feirtag, 1986; Swanson, 1992, 1999). Other findings demonstrated brainstem visceral projections to the cortex, and direct projections from the neo- and pallocortex to brainstem sites have direct control of viscera function (Norgren,
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1995; Saper, 1996; Swanson, 1992). Visceral information from the heart and gastrointestinal organs can reach the amygdala and insular cortex within one or two synapses from the solitary and parabrachial nuclei of the brainstem (Allen, Saper, Hurley, & Cechetto, 1991; Saper, 1982). Our notion of the limbic system (Broca, 1878; MacLean, 1949; Papez, 1937) has also continued to evolve to the point where a unitary limbic system for emotion is questioned for its validity (Herbert & Schulkin, 2002; LeDoux, 1996; Saper, 1996; Swanson, 2000). There is, however, a visceral neural axis. In both chemical and functional terms the visceral nervous system information traverses all levels of the nervous system, from regions of the solitary tract and parabrahical nuclei to the amygdala and bed nucleus of the stria terminalis and regions of the neocortex (Allen et al., 1991; Norgren, 1995; Saper, 1996; Swanson, 2000). In contrast to a unitary emotional system, there are likely numerous circuits for different types of emotions (Calder, Lawrence, & Young, 2001; Ekman & Davidson, 1994; Lane & Nadel, 1999). Some circuits may be parallel (e.g., fear and joy), while others more integrated for particular emotions (e.g., fear and anger). These circuits are likely not segregated but use bits and pieces of circuits of one emotion for circuitry of other emotions. For example, the circuitry of the amygdala is an integral component of many types of fear, but may also be used to modulate anger-like behavior that may primarily be a function of other circuits (Calder et al., 2001; Rosen & Schulkin, 1998) e.g., septum-hypothalamus (Gray, 1982). The amygdala is also importantly linked to a number of functions other than fear (Emery et al., 2001; Gallagher & Holland, 1994; Davis & Whalen, 2001; Schulkin, 1991, 1999: social appraisals, reward, attention, appetite). Similarly, neural circuits involved in emotions may also subserve other functions. The amygdala is a major component of taste/visceral connectivity to the brainstem and these visceral pathways underlie motivated behavior (Herrick, 1905; Norgren, 1995; Pfaffmann, Norgen, & Grill, 1977; Spector, 2000). Importantly, many of the neuropeptides that play a key role in the organization and expression of adaptive responses are found along the gustatory–visceral axes. Neuropeptides, for example, such as angiotensin and corticotropin releasing hormone (CRH) or oxytocin are found in many of the sites along the taste/visceral pathways (Gray, 1999; Lind, Swanson, & Ganten, 1984; Swanson, 1992). The chemical pathways also play vital roles in the organization of emotions and they are represented in both the peripheral and central nervous systems (see Fig. 2). While all neurotransmitters play a role in the organization of central states, we want to use the neuropeptides as illustrative examples of how the peripheral
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Fig. 2. The three drawings from top to bottom: corticotropin releasing hormone (CRH) in the brain (Swanson, Sawchenko, Rivier, & Vale, 1983), angiotensin sites in the brain (Lind et al., 1984), and the central gustatory neural axis (Norgren, 1995). The point one should note is that many of the peptide sites overlap with gustatory–visceral sites in the brain.
Fig. 3. Repeated systemic administered corticosterone (CORT) given before training enhances long-term memory for contextual fear conditioning. The mean SEM percent time spent freezing was measured immediately after the training (post-shock) or in a retention test 24 h after conditioning (retention). There were no differences in post-shock freezing, while freezing in the retention test was significantly facilitated by repeated CORT (shown in the figure). The * denotes that in the Vehicle group freezing during the retention test was significantly different from post-shock freezing. (Digitized images of corticotropin releasing hormone (CRH) mRNA in the central nucleus of the amygdala (CeA; arrows) 2 h after the last of twice daily VEHICLE or CORT injections for 5 days.) CRH mRNA in the CeA was significantly increased by repeated CORT administration (p < :02). One mechanism to increase vigilance, attention and memory is the upregulation by CORT on CRH neurons within the visceral neural axis that are organizing the behavioral responses associated with fear (Thompson et al., 2000).
and central systems can use the same endogenous chemicals. Nature is opportunistic to use the same sets of molecules to subserve systemic physiologic representation and central organization of behavior. For example, oxytocin in the septum and bed nucleus of the stria terminalis is linked to attachment behaviors; in the periphery they are involved in milk letdown and lactation (Carter, 1998; Insel, 1992). The central expression of oxytocin, as a neuropeptide, is linked to decisions to approach or avoid objects and is mediated by regions of the brain which may include the amygdala, bed nucleus of the stria terminalis and no doubt influencing regions of the frontal cortex (Carter, Lederhendler, & Kirkpatrick, 1997/1999; Insel, 1992). Attachment behavior is a fundamental way in which children and many other kinds of animals (Bowlby, 1988; Hofer & Sullivan, 2001; Tinbergen, 1951) get oriented to the world and find security. The appraisal mechanisms may often be reflexive and fast (Oatley & Jenkins, 1996), but with age and experience perhaps less so. The states of fear and alertness to external events have been linked to extra-hypothalamic expression of the neuropeptide CRH, particularly in the central nucleus of the amygdala and the bed nucleus of the stria
terminalis (e.g., Gray, 1999; Lee & Davis, 1997; Schulkin, 1999). Along the visceral neural axis is information related to autonomic and behavioral adaptation and CRH expression is linked to appraisal of events that are linked to danger, or novelty (Davis & Whalen, 2001; Habib et al., 2000; Kalin, Shelton, & Davidson, 2000; Rosen & Schulkin, 1998). The expression of CRH is also linked to frontal neocortical activation (Kalin et al., 2000). Importantly, input from peripheral sites, such as the adrenal gland (and the production of cortisol or corticosterone), acts to facilitate neuropeptide expression CRH. One result is to facilitate a central state of fear (Corodimas, LeDoux, Gold, & Schulkin, 1994; Thompson, Schulkin, & Rosen, 2000) (see Fig. 3). Another neuropeptide, that underlies visceral expression and that is fundamental in generating a behavior, is angiotensin. Angiotensin is essential for thirst and sodium intake, including the central state of search, recalling past associations and feeling satisfied when ingesting water or sodium (Denton, McKinley, & Weisinger, 1996; Fitzsimmons, 1999). Angiotensin plays diverse roles in the periphery essential for maintaining body fluid balance, while in the brain it is essential for organizing behavioral responses. Thus, angiotensin
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expression in the brain is important for palatability and affective appraisals for body fluid regulation. There is nothing abstract and divorced about the representation of fluid balance at a number of levels within the visceral neural axis (Fitzsimmons, 1999; Herbert & Schulkin, 2002). Each of these neuropeptides serves both physiological and behavioral regulation. They are information molecules (Herbert & Schulkin, 2002; see also Berridge & Robinson, 1998 and Schultz, Tremblay, & Hollerman, 2000 for a discussion of a neurotransmitter) in the visceral nervous system that are essential for behavioral viability. These three examples, and there are a number of others (Carter et al., 1997/1999; Schulkin, 1999), contribute importantly to both peripheral autonomic and central representations in the organization and expression of the emotions.
4. Emotions and the regulation of the internal milieu: Hedonic experiences Adherents of the tradition of regulatory physiology understood that behavior is vital to sustain internal homeostatic balance and adaptations to perturbation (Richter, 1976). Central states of the brain, informed by visceral representations, guide behavioral responses (Stellar, 1974). These are not divorced abstract representations that discard the body, but the body informs the brain allowing it to respond appropriately (Denton et al., 1996). Alterations in homeostatic balance and internal physiology impact the brain to generate behaviors, to ameliorate discomforts, and so forth. Brains of many animal species have evolved to a point where neural information processing systems are designed to not only respond to internal changes but to anticipate them. Along with anticipation, the intensity of internal stimulation, and the memory of the intensity, is a fundamental trigger in approach or avoidance mechanisms (Schnierla, 1966). Judgements to approach or avoid reflect the activation of the brain circuits throughout the neural axis. Circuits involving the frontal cortex (e.g., Davidson et al., 1990; Schmidt & Fox, 1999), the striatum (Calder et al., 2001; Saper, 1996; Schultz et al., 2000), amygdala and hypothalamus (LeDoux, 1996; Saper, 1996; Stellar & Stellar, 1985; Swanson, 2000) and brainstem regions, to give a few examples, are all essential for carrying out the full range of behavioral responses. A wide variety of objects (foods, people, and settings), either learned or not learned, are powerful elicitors of approach behaviors. These approach behaviors are importantly linked to palatability judgements and appraisal mechanisms (i.e., what something looks like, what it tastes like, if it is sweet, if the texture is soft, if the body is inviting). We would suggest that preferences
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Fig. 4. Gluttonous pleasurable experience, and unfortunately associated with the lack of control and the expression of the emotions.
do in fact need inferences (cf. Lazarus, 1991; Sabini & Silver, 1998; Zajonc, 1980, 2000), they are just low-level appraisal systems (discussed in following section). Hedonic experiences linked to palatability judgements are also important features that motivate behavior (e.g., Berridge, 1996, 2000; Pfaffmann et al., 1977; Stellar, 1974). A question is whether emotional and hedonic experiences are the same or not. Both inform, both motivate and organize behavior. Nevertheless, hedonic experiences are not identical with emotions. For example, love (an emotion) is not an orgasm, but orgasms are awfully motivating (see Fig. 4). It has also been suggested (Sabini & Silver, 1998) that motivation should replace emotions in our scientific lexicon. In this view, motivation (the search for sodium, avoidance of fear-related events, etc) is adaptive, but emotions are not (see also Sartre, 1948). In a more integrated adaptive-functional view, motivations are also mechanisms for survival and are related to emotions, but distinct from emotions. What is important to note is that some rich traditions did not commit ‘‘DescartesÕ Error’’ (Damasio, 1994) of dissociating cognition from bodily experience. Those concerned with information processing within physiological systems essential for homeostatic (e.g., body temperature, fluid balance) and non-homeostatic (e.g., defensive) functions did not detach the impact of bodily experience from real world decisions (Garcia, Hankins, & Rusiniak, 1974; Richter, 1976; Stellar, 1974). Some of the circuits for emotional expression are also utilized in the organization of behaviors important for maintaining homeostatic and non-homeostatic systems.
5. Is emotional processing cognitive or non-cognitive? There is a well-known controversy about whether the emotions are cognitive or pre-cognitive processing. We believe emotional processing is cognitive. This does not mean that emotions are necessarily conscious or the cognitive processes are transparent to the individual. Just as neural processing and machinations of other cognition systems are unconscious, so are those of emotions. Appraisal occurs in all emotional responses (Ekman, 1992; Pinker, 1997). Appraisals, either nonemotional or emotional, can be fast and automatic such
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as the recognition of syntax, or the recognition of a happy or sad face (Young, 1998). The fact that the appraisal of both types of stimuli can be fast suggests that the mechanisms of information processing are evolutionary prepared to respond to certain sorts of stimuli, and that certain kinds of prepared learning and associations are intrinsic to problem-solving (Rozin, 1998). Fast- or slow-acting systems designed to enhance problem-solving are not perfect systems, and do not need to be perfect in order to be legitimate and selected by evolution (Gigerenzer, 1991; Simon, 1979, 1982; Todd & Gigerenzer, 2000). Emotions are no less cognitive aids than other forms of problem-solving. However, what makes emotions special is the intimate relationship of appraisal mechanisms and response or output systems. Brain mechanisms of appraisal and response of a particular emotion are parts of an integrated circuitry. For example, with the emotion of fear, appraisal mechanisms are partially embodied in the lateral and basal nuclei of the amygdala and output is initiated in the adjacent central nucleus of the amygdala (LeDoux, 1996, 2000; Swanson & Petrovich, 1998). Connections from the appraisal mechanisms directly project to the output pathways. In other words, with appraisal mechanisms so intimately tied to emotional output/behavioral responses it would be very difficult to evaluate an emotionally provoking stimulus without having a tendency to act or produce an actual overt response. Importantly, this is different from nonemotional cognitive processing like language, where input processing (WernickeÕs area) is connected but not adjacent or intimately integrated with the motor output of language (BrocaÕs area) and can be dissociated by lesions or brain damage. Automatic and evolutionarily conserved emotional appraisal may be exemplified by recent studies demonstrating that predator odors elicit fear-like responses in rats that have never experienced these odors before (Dulac, 2000; Wallace & Rosen, 2001). The first time rats are presented with an odorant isolated from fox feces they display avoidance and fear-like behavior, suggesting that laboratory rats have unconditioned fear to predator odor. Furthermore, lesions of the amygdala that impair learning of conditioned fear as measured by freezing behavior have little effect on unconditioned freezing to the predator odorant (Wallace & Rosen, 2001). The effects of amygdala lesions cannot be at the level of behavioral output because freezing to the predator odor was robust in amygdala-lesioned rats. The amygdala lesion likely disrupted appraisal and learning and memory mechanisms for conditioned fear. Thus, while learned fear may need the amygdala for appraisal of conditioned fear stimuli, appraisal of unconditioned fear of predator odor may occur at other levels of brain (Fendt, Endres, & Apfeobach, 2003), possibly even as early as the sensory mechanisms for olfaction.
Does the fast, automatic and possibly innate processes of emotions denigrate them? Does it make them less cognitive than deliberate thought? We think not. Cognition should not be viewed narrowly as conscious information processing, but as processing that can have multiple levels from simple habituation and sensitization to willful, conscious, decision-making. Moreover, we are not denying the experience of the emotions, in fact, the experience is part of the transaction with the environment (Dewey, 1925/1989; Schulkin, 2000), the experience of fear, joy, delight, etc. To say that the emotions are part of the biological mechanisms of information processing systems is not to denigrate them or leave the experience out of the explanation. It makes emotions ripe for scientific inquiry at multiple levels of analysis.
6. Conclusion Advances in the behavioral/cognitive and neural sciences have expanded our understanding of the mechanisms and functions of the emotions. The emotions are vital for information processing of many stimuli and experiences. There certainly are differences in the brain related to different kinds of information processing in cortical and sub-cortical areas involved in emotions and other kinds of events (Bush, Luu, & Posner, 2000; Calder et al., 2001; Davidson, Putnam, & Larson, 2000; Dolan, 2000; Price, Carmichael, & Drevets, 1996). We have emphasized that the viscera and numerous levels of the neural axis are involved in information processing subserving different and overlapping functions with regard to the emotions. For example, the amygdala and the prefrontal cortex subserve different functions in the appraisal and analysis of fear-related stimuli (Bechara et al., 2000; Calder et al., 2001; Wright et al., 2000). And importantly, the amygdala may be activated when one looks at something fearful, imagines something fearful, or reads a sentence about something fearful. While the experience of feeling is intrinsic to human emotions, we prefer the language of diverse appraisal systems (Dewey, 1925/1989; Goldman, 1986; Lazarus, 1991) when describing the emotions, as opposed to feelings that are distinct from cognition. The debates about separating feeling from cognition are endless, and perhaps not fruitful. Affective computational systems or appraisal–response systems would seem a good way to describe emotional processing and promote empirical study on emotions. Appraisal mechanisms are pervasive to systems of both approach and avoidance, and are thus parts of emotions, motivations, and central states. Appraisals may be low level, and certainly unconscious in terms of mechanisms of action. Moreover, appraisal systems do not sit at one level of the brain (cortex) and pure reception at another (brainstem); filter systems, encoding
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systems receptor fields, are pervasive throughout the nervous systems. The language of appraisal should not be rarified in cortical space; it exists in the lower brainstem (e.g., solitary and parabrachial nuclei). But to say that the emotions are informational systems is not to say that this is all they are. And we hope that by continually demythologizing the emotions they do not become either elevated or denigrated, but our understanding and appreciation of these very important aspects of life that were favored during our evolutionary development are enhanced.
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