The significant role of emotions in evolution and adaptation suggests that there must be more than 1 mechanism for generating them. Nevertheless, much of current emotion theory focuses on cognitive processes (appraisal, attribution, and construal) as the sole, or primary, means of eliciting emotions. As an alternative to this position, the present model describes 4 types of emotion-activating systems, 3 of which involve noncognitive information processing. From an evolutionary-developmental perspective, the systems may be viewed as a loosely organized hierarchical arrangement, with neural systems, the simplest and most rapid, at the base and cognitive systems, the most complex and versatile, at the top. The emotion-activating systems operate under a number of constraints, including genetically influenced individual differences. The hierarchical organization of the systems for generating emotions provides an adaptive advantage. Rafe's friends always describe him as a happy person. He likes to play tennis and finds great enjoyment in watching the top professionals play the game. After watching his favorite player win in the semifinals of a grand prix tennis tournament, Rafe contentedly stood in line under a hot August sun waiting to get a cool drink. As the glow of his vicarious victory faded, the heat and humidity became more and more oppressive. Suddenly, Rafe felt a piercing pain from a blow to his lower back. Rafe turned rapidly with an angry expression and clenched fist. Rafe saw that he had been hit by Rebecca, a person with hemiplegia whose wheelchair had gone out of control and caused her to crash into Rafe and to spill her drink on her dress. Rafe's understanding that the cause of his pain was an uncontrollable event that had embarrassed Rebecca immediately changed his anger to sadness and sympathy. Though still in pain, his happy nature surfaced, and he began helping Rebecca recover from the accident. According to the present model, Rafe's normally happy disposition is a function of a genetically influenced neural system that operates more or less continuously to generate his characteristic emotional state. The background neural activity responsible for Rafe's trait emotionality (i.e., happy mood), the changes in his emotions system that were due to neurochemical activity instigated by the ambient temperature, the affective/ pain processes that led to anger, and the amplification of his anger by sensorimotor/expressive actions required no cognitive mediation. All of these emotion-activating and regulatory systems can operate in very young infants, probably before they This work was supported by National Science Foundation Grant BND8706146. I am grateful to Brian Ackerman, Steven Grant, Paul Harris, Helene Intraub, John McLaughlin, Ira Roseman, and Thomas Scott for their helpful comments on a draft of this article. Correspondence concerning this article should be addressed to Carroll E. Izard, Department of Psychology, 220 Wolf Hall, University of Delaware, Newark, Delaware 19716. are capable of engaging in cognition based on representational processes and memory (Harris, 1983b ). Rafe's perception of the visual scene engaged the emotion-activating processes of his cognitive systems, resulting in appraisals, causal attributions, judgments, and appropriate emotion responses. In the present scenario, his perception of the visual scene led him to attribute the cause of his pain to an uncontrollable event that had actually embarrassed and hurt the causal agent, Rebecca. These appraisal and attributional processes changed his anger to sadness and sympathy. The cognitive systems for emotion activation accounted for the third emotion that Rafe experienced. His characteristically happy mood and the pain-activated anger were products of noncognitive emotion-activating systems, which together with cognition are capable of generating emotion responses for all contingencies. The nascent idea of alternative routes to emotion activation has been in the shadows of a growing set of theories that focus primarily on cognitive processes. Yet, emotions are so basic to the evolution and adaptation of human beings (Darwin, 1872 (Darwin, / 1965 Hamburg, 1963; Izard, 1989; Nesse, 1990; Plutchik, 1980; Zajonc, 1980) that it would seem obvious that evolution and the brain's penchant for redundancy (Mayr, 1988; Valenstein, 1973) would have guaranteed the existence of multiple processes for generating them. This compelling notion has not yet motivated a comprehensive theory that attempts to specify the various emotion-activating processes. This is true despite the fact that there are a number of theorists who acknowledge different types of emotion activators and a growing body of relevant data (for reviews, see Izard, 1990; Zajonc, Murphy, & Inglehart, 1989) . The increasingly wide acceptance of emotions as motivational processes that influence cognition and action (Anderson, 1989; Harris, 1989; Lazarus, Kanner, & Folkman, 1980; G. A. Miller & Johnson-Laird, 1976; Neisser, 1976) underscores the need for a theoretical framework for understanding their activation. Another reason for a comprehensive model of emotion acti- vation is the need to gain some perspective on the importance of cognition in generating emotions. There is a growing interest in research on emotion-cognition relations, but it does not seem possible to analyze or predict such relations until there is a framework for examining the relative contributions of cognitive and noncognitive elicitors of emotions. If, on the one hand, cognition were always the cause as well as a constituent of emotion (Lazarus, 1991; Ortony, Clore, & Collins, 1988) , there would be some restrictions on the ways that cognition and emotion could relate. Emotions could not be considered as qualitatively distinct independent variables (Izard, 1965; Zajonc, 1980) . On the other hand, if emotion can be denned as something other than a cognition-dependent phenomenon and if cognition is but one of several types of emotion-activating processes, then there can be a greater range of relations between emotion and cognition. For example, noncognitively activated emotions could generate and interact with cognition. A prominent emotion theorist (Lazarus, 1991) has continued to maintain that "cognitive mediation is a necessary condition of emotion" (p. 356). He argued that even drug-induced emotions and emotions processed entirely through subcortical structures and pathways are mediated by cognition. Indeed, Lazarus held that discussion of noncognitive activators of emotion "keeps us from asking the right questions, which have to do with the kinds of cognitive activities that are causally involved in the emotion process" (p. 357). To maintain this position, Lazarus (1984) held that the simplest perceptual phenomenon, inputs without full-fledged denotations, can constitute cognitive appraisal that generates meaning, evaluative judgment, and emotion. Another cognitive theory of emotion takes a stand similar to that of Lazarus (1984 Lazarus ( ,1991 . It phrases the causal process a bit differently, maintaining that emotions are a function of the person's construal of salient features of the context (Ortony et al., 1988) . The authors of this theory held that of four types of data relating to emotions, only language and self-report are to be considered in the generation of emotion experiences. They "largely ignore behavioral and physiological evidence" on the grounds that they are "consequences or concomitants of emotion states" (p. 14). A similar position is that "emotions result from meanings, and meanings, to a large extent, from inferred consequences or causes" (Frijda, 1986, p. 310; also see Frijda, 1988). Although Frijda (1986) and other cognitively oriented emotion theorists have acknowledged that brain stimulation can elicit emotion, neither this nor any other noncognitive variable plays a significant role in their treatment of emotion activation. For example, Frijda discussed "neurophysiological mechanisms involved in emotional phenomena" as " 'conditions' for emotion" (p. 379) rather than as a neural system capable of independently activating emotions. These strong views on the peremptory role of cognition in emotion activation raise two critical questions. First, can cognition be defined by some conceptual boundaries such that it can be understood as something more specific to mental representation and memory than the very broad concept of information processing? Second, if cognition is conceived as antecedent to emotion, then what drives cognition? Contrary to Lazarus's (1984 Lazarus's ( ,1991 position, some theorists have maintained that it is not heuristic to define cognition so broadly as to include all information processing (Hoffman, 1985; Izard, 1989 Izard, ,1992 Zajonc, 1984) . Several kinds of information processing are going on in all organisms all the time. Surely it is not helpful to conceive of information processing in DNA molecules as cognition. Although all cases of emotion activation involve information processing, in some cases, according to the present model, the information processing that generates emotion is noncognitive. A challenge for cognitive scientists is to draw some working boundaries around the domain of cognition. Without such boundaries and without clear specification of the mechanism for cognitive mediation, arguments regarding cognition as the necessary cause of emotion will be without strong foundation. Hoffman (1985) has attempted to resolve the question of the necessity of cognition in emotion activation by delineating several different modes of information processing that mediate affect arousal. He discussed these modes in the order in which they emerge in development. The first mode to emerge, direct response to the physical features of a stimulus, may not be a function of cognition if any restrictions are put on that term. This first mode of emotion activation, according to Hoffman, requires only "registration of the stimulus event and a minimum of perceptual organization" (p. 246). Although only a few theorists take the extreme position that cognition is a necessary antecedent of all emotion experiences, most theories of emotion activation and most of the related empirical research are concerned only with cognitive concepts. From the existing literature, students of emotions can gain the impression that an understanding of cognitive operations such as appraisal and attributional processes gives them an adequate knowledge of the causes of emotions. There are several theories that provide a good description of these processes (e.g., Frijda, 1986; Scherer, 1988; Smith & Ellsworth, 1985) . Some of these theories allow for the possibility of other avenues to emotion, but they inspire only studies of cognitive causes and thus give the impression that cognition accounts for virtually all the emotions of human experience or, at least, the most important ones. Weiner's (1985) social-cognitive (attribution) theory of emotions is an exception to the foregoing characterization of cognitive theories of emotions. His theory explains the generation of emotions as a function of causal ascriptions, but it acknowledges that certain emotions (e.g., excitement, joy, and disgust) are not necessarily, or even primarily, mediated by perceptions of causality. Perhaps the most significant issue here is not whether cognition is the exclusive determinant of emotions but whether there are viable alternative hypotheses for emotion activation and whether noncognitive activators account for a substantial amount of the emotions experienced in daily life. I shall argue that there are numerous specific activators of emotions and that they fall into four broad classes: neural (noncognitive evaluative processes), sensorimotor, motivational, and cognitive. The classes of activators constitute four separate but highly interac-70 CARROLL E. IZARD tive systems. Thus, cognitive operations constitute one of the four classes of emotion-activating processes, but whether cognition accounts for more emotions than any other class of activators, or more than all the other classes combined, is an empirical question. I shall discuss possible limitations on cognition as the primary cause of emotion. This discussion will involve a consideration of individual differences that might be expected to influence appraisal processes and emotionality through noncognitive information processing. On the Need for a Concept of Noncognitive Information Processing For the purpose of discussing cognition as an emotion-activating system and for studying emotion-cognition relations, I suggest some working boundaries or distinctions among varieties of noncognitive and cognitive information processes. Some such distinctions are necessary to consider the possibility that emotions are generated by truly different processes. Surely, part of the difference between cognitive and biosocial theories on the issue of emotion activation is a function of their different conceptions of cognition and their different views on the heuristic value of conceptually separating emotion and cognition, information processing and cognition, and noncognitive and cognitive information processes. The problem of definition or boundary setting is made more complex by the existence of some seemingly overinclusive definitions of cognition (see the Lazarus-Zajonc debate, Lazarus, 1984; Zajonc, 1984) . Furthermore, there are many different types of cognition: automatic as contrasted with deliberate ; conscious as contrasted with unconscious, preconscious, and subconscious (Kihlstrom, 1987; Kihlstrom & Hoyt, 1990) ; cognition at different levels of awareness (Bower, 1990) ; and cognition in repression and dissociation (see Singer, 1990). Building on earlier work on subliminal perception and the distinctions between forms of episodic memory, Kihlstrom (1990) has made a case for implicit cognition (implicit perception, implicit learning, and implicit memory) that might lead to "implicit emotion." There is impressive evidence and argument for all the foregoing types of cognitive processes, and, considered together, they make for a very broad conception of cognition. Even with cognition defined to include all the foregoing types of mental activities, however, it is misleading to equate it with information processing. The study of information processing in the genes ofDmsophila melanogasterhas made great contributions to understanding the human genome, but it has not enlightened us on human mental life. Not only does it seem proper to exclude the decoding of information in amino acids, enzymes, and genes from the cognition of cognitive psychology, it may also be appropriate to exclude that which guides reflexive, instinctive, and biologically prepared or genetically disposed behavior. Thus, a central thesis of the present article is that cognition, defined as dependent on some form of learningor experience-based memory, does not include all the forms of information processing that lead to emotion. Clearly, information processing consists of several types or levels of data decoding and synthesis, ranging from that which leads to the color of an eye to that which produces a Mona Lisa or a theory of relativity. All these kinds of information processing may lie along a single continuum. To paraphrase Sinnott (1966) , who can say when the information processing involved in the chick's embryological development ends and that which mediates its behavior and mental life begins? When it starts pecking its way out of the shell? When it perceives the mother hen and imprinting results in following behavior? When it imitates her scratching movements in search of food? When it flees from the shadow of a hawk? When its behavior is guided primarily by sensory data from the environment? Some of the foregoing chick activities, including fear behavior and flight, are guided, in part, by information encoded in the genes and, in part, by sensory input from the environment. Therein may lie a clue to a boundary or distinction between noncognitive and cognitive information processing. One possibility for marking the boundary is to identify behaviors that are instinctive, that are instinctlike, or that are elicited by particular environmental features (Schneirla, 1965) , biologically prepared or genetically disposed stimuli (Rozin & Fallen, 1987; Seligman, 1970) , or "natural clues" (Bowlby, 1973) . Such information leads to a number of emotion responses in animals, young infants, and children (Bowlby, 1973; Gray, 1971; Izard, Hembree, & Huebner, 1987; Stenberg & Campos, 1990) . Infants of 3 weeks smile at a human face and display anger in pain at 8 weeks and anger at restraint at 16 weeks. In all of these conditions, infants undoubtedly process information that leads to the emotion response, but such processing does not constitute cognition as defined here. The infants detect a pattern of light, lines, or neurochemical changes and experience an emotioneliciting pattern of stimulation (which is probably mediated subcortically), but these phenomena do not require cognitive representation, memory, matching, or comparison processes. Infants of 3 to 8 weeks of age are probably incapable of such mentation (Harris, 1983b) . The arbitrariness of any answer to Sinnott's (1966) question as to where embryological growth ends and cognition and behavior begin suggests the reasonableness of a concept of a single continuum of information processing. Whether the underlying phenomena are points on a continuum or discrete classes, for purposes of discussing cognitive versus noncognitive processes and considering cognition as an activator and correlate of emotion, I propose four differentiable sorts of information processing: cellular, organismic, biopsychological, and cognitive. These may be conceived as segments on the grand continuum, but because my goal here is to show significant differences among them, I refer to them as categories or types. The first three of the foregoing categories involve types of noncognitive information processing. The cellular category is exemplified by information processing in enzymes and genes. Such processing has no direct relation to sensory input or the cognitive processes that depend on sense data. The information processed at the cellular level was encoded through natural selection in the evolution of the species. Cellular processing FOUR SYSTEMS FOR EMOTION ACTIVATION 71 does not directly affect cognition and action. Cellular information processing does play a significant role in determining emotion thresholds and proneness to experience certain emotions, and thus it is a major determinant of an individual's characteristic mood. Furthermore, as I argue later, the individual differences rooted in cellular information processing place constraints on organismic, biopsychological, and cognitive information processing. Organismic information processing that leads to emotion also involves biological information coded in the genes during the course of evolution. In some cases, biological information is processed with little or no sensory information from exteroceptors. However, organismic information processing often involves sense data from interoceptors, and the primary sources of such information are physiological drive states. Examples of emotion activation through organismic information processing are pain-activated anger (Berkowitz, 1990; and taste-elicited disgust (Steiner, 1979) . Biopsychological information processing that activates emotions involves an interaction of biological information processing and the processing of information derived through learning or experience, that is, an interaction between organismic information processing and acquired knowledge (cognition). The processes involved in the interaction of these two types of information and the subsequent effect on emotion activation may be roughly analogous to the processes involved in the interaction of implicit and explicit memory and the subsequent effect on conscious processes (Kihlstrom, 1980; Kihlstrom & Hoyt, 1990) . Kihlstrom showed that memorized words that were rendered nonrecallable (or relegated to implicit memory) through posthypnotic suggestion were still available for use in response to words previously associated with them. In similar fashion, genetically coded information relevant to evolutionarily significant stimuli, though unavailable to consciousness, interacts with information derived through cognitive processes to determine the specific emotion response. Although biopsychological information processing requires cognitive evaluation of sensory input from the environment, the critical database is biological information from evolution. (For a discussion of genetic constraints on "what can be learned, hence what can be attended to, and thence what can be perceived," see Shepard, 1984, p. 432). This category of information processing is exemplified in biologically prepared or genetically disposed fear and disgust responses (Lanzetta & Orr, 1986; Mineka, Davidson, Cook, & Keir, 1984; Rozin & Fallen, 1987; Seligman, 1970) . Evidence suggests that it is the critical contribution of biological information to prepared or evolutionarily influenced fear responses that makes their acquisition more likely and their extinction slow and difficult. Although McNally (1987) argued that the data relating to acquisition and extinction are inconclusive, he acknowledged that fears of evolutionary significance are overrepresented in human phobias. Following Bennett- Levy and Marteau (1984) , he concluded that humans may be biologically prepared to learn to fear certain perceptual features embedded in phobic stimuli. This suggests that emotions activated by such stimuli might require only feature detection. Even when more complex cognition is involved in biopsychological information processing that leads to emotion, cognition may not be the dominant determinant of the emotion response. The primary cause may be a genetically determined predisposition. Biopsychological information processing could be considered a special subtype of cognition. It can involve a variety of cognitive processes. Perhaps the choice of category label should follow a determination of which type of information is dominant in determining a specific emotion response. In any case, emotion activation through the interaction of biological information processing and the processing of individually acquired information invokes the idea of an information-processing continuum. The cognitive category includes all mental processes that depend on acquired representations, those representations derived from the learning and experience of the individual. Cognition, as defined in differential emotions theory (Izard & Malatesta, 1987) and in the present model of emotion activation, begins at that point on the information-processing continuum where learning or experience produces mental representations and memory sufficient to mediate comparison processes and discrimination. It is when these, as well as higher order mental processes, are involved in assessing stimulus information that cognition can, though not necessarily, play a dominant role in emotion activation. Possibly the cognitive category (or cognitive segment of the information-processing continuum), as defined here, is sufficiently broad to include the types or levels of information processing of interest to cognitive psychologistswhether simple discrimination or complex symbol manipulation; automatic or deliberate; conscious or unconscious, preconscious, or subconscious; and whether in repression or dissociation. Such a range of differentiable types of noncognitive information processing has not been discovered (or much sought), but it is known to vary from simple to complex. Something of the extent of its complexity is illustrated by Lorenz's (1965) description of the instinctive behavior of the young swift. Although reared in a cave too narrow for it to extend its wings and too shallow for it to obtain a sharp retinal image, the swift can, on its first flight, assess distances by the parallactic shift of the objects' images; cope with air resistances, upcurrents, and air pockets; recognize and catch prey; and make a precise landing in a suitable place. I emphasize that the foregoing treatment of cognition is a special-purpose one. Its primary function is to facilitate the discrimination of cognitive and noncognitive information processing and the discussion of emotion-cognition relations and cognition as an emotion-activating system. Before presenting a multisystem-multimodal model of emotion activation, it is necessary to say something about what is being activated. This brings us to a very thorny issue, defining emotion, and it will not be resolved to everyone's satisfaction. Although an attempt at a complete definition would certainly create controversy, it is possible to identify basic characteristics of emotion on which there is considerable agreement. Everyone agrees that emotions involve particular neural processes. Several neuroscientists have identified mechanisms, 72 CARROLL E. IZARD pathways, and neurotransmitters for emotion in general or for specific emotions (e.g., Aggleton & Mishkin, 1986; Kling, 1986; LeDoux, 1987; Panksepp, 1986; Rolls, 1986) . They are not in complete agreement, but they share considerable common ground. They agree that the neural substrates of emotions are best described as circuits or networks of structures and not as localized brain centers. Two pathways for the activation of fear are depicted in Figure 1 . The important point here is that particular neural substrates can be identified and that an emotion is not so general a process that all brain structuresand neurotransmitters are equally involved. Thus, as research technology improves, it should become possible to index emotions in terms of increasingly specific neural systems. A substantial number of emotion researchers agree that emotion includes an expressive or motor component or, at least, an efferent activity in the central nervous system (e.g., Ekman, 1984; Izard, 1991; Lang, 1984; Leventhal, 1984; Plutchik, 1980; Tomkins, 1962) . If an action tendency is conceived as involving expressive or efferent processes, several other theorists could be included in the consensus on this point (e.g., Arnold, 1960; Bull, 1951; Cacioppo, Martzke, Petty, & Tassinary, 1988; Frijda, 1986; Lang, 1984) . In any case, it is clear that many emotion researchers agree that particular expressive movements or action tendencies help define emotion. Furthermore, some of these investigators have developed precise and objective methods, including observational (Ekman & Friesen, 1978; Izard, 1979) and psychophysiological techniques (Cacioppo & Tassinary, 1990; Lang, 1979) Finally, all researchers, from clinical investigators to neuroscientists, agree that emotions register in consciousness. Indeed, since William James (1884) identified the feeling of certain bodily changes as the quintessence of emotion, many writers use the terms emotion, feeling, and emotion experience interchangeably. Although James made a persuasive case for considering the experiential component as the quintessence of emotion, the use of the term emotion when referring only to emotion experience ignores the other components and is, thus, imprecise and misleading. There is disagreement on the nature of the experiential component of emotion, but most definitions include one or more of the following: 1. Motivation 2. Action readiness 3. Action tendency 4. Perceptual selectivity 5. Cues for cognition and action 6. Feeling state. Although all these terms may not apply equally to all emotion experiences, I propose that all of them are acceptable ways of identifying aspects of the third component of emotion. One could argue that the common denominator among the descriptors of emotion experience is a noncognitive motivational condition or process in consciousness that normally, after language acquisition, can be accessed and verbally reported, albeit imprecisely. However, when the cognition associated with an emotion experience has been repressed or relegated to a lower level of awareness, retrieval (accessing or labeling) may require the aid of appropriate cues (Bower, 1990) . One possible exception to the foregoing reportability rule is the individual with a represser personality type, who is apparently capable of dissociating the conscious aspects of emotions, especially the negative emotions in anxiety, even when psychophysiological indexes indicate that there is emotion arousal (see Schwartz, 1990; Weinberger, 1990) . There are two possibilities here. There may be no specific emotion experience because the arousal is undifferentiated, or an emotion experience is present but special retrieval cues and procedures are necessary to obtain a veridical verbal report. Although there may be exceptions, it seems reasonable to stay with the notion that emotion experience, or the third component of emotion, can be identified as a motivational condition or process in consciousness that manifests itself as action readiness, action tendency, a biasing of perception, cues for perceptual-cognitive processes, or a feeling state. In this context, motivational condition is conceived as a property inherent in the activity of the neural substrates of emotion or as a direct product of neural processes. In differential emotions theory (Izard, 1971 (Izard, , 1977 , the theory underlying the present model of emotion activation, an emotion is distinguished from a drive state. As Tomkins (1962) has argued, drives, such as hunger, thirst, sex, and the need to eliminate, are cyclical in nature, and each one is associated with and satisfied by a relatively restricted range of stimuli. The satisfaction of a drive state requires activity in peripheral organs FOUR SYSTEMS FOR EMOTION ACTIVATION 73 dedicated to, or at least associated with, the drive system. Drives provide specific information regarding the time and place that something needs to be done and cues a relatively specific set of responses. In contrast, an emotion has no temporal cycle, is not dependent on peripheral physiological processes, can be associated with a virtually limitless variety of phenomena, and can motivate an equally wide range of cognitions and actions (Tomkins, 1962) . In contrast to emotion feelings, feelings that derive from drive states are influenced by cyclical input from visceral organs innervated by the autonomic nervous system (ANS). Time is a stable source of variance in the intensity of drive states, whereas any number of variables (e.g., stage of development, nature of the eliciting stimulus, unconscious cognitive processes, or personality defense mechanisms such as repression) may, independently of time, contribute to variations in the intensity of emotions. Mood is substantively synonymous with emotion but may be used to refer to emotion that is sustained over a relatively long period of time (cf. Mandler, 1984). In differential emotions theory, affect and motivation are interchangeable terms that refer to all motivational phenomena-emotions, drives, and affective-cognitive structures. Fundamentally, emotion is about motivation-positive and negative feelings, readiness or tendency to cope, and cues for cognition and action. Cognition is about knowledge-learning, memory, symbol manipulation, thinking, and language. Perception, when it leads to representation and memory, is clearly part of cognition. Subcognitive perception, or perception that does not result in memory (cf. Zajonc, 1980), may operate primarily in the service of the emotions system. The foregoing working definitions of emotion and cognition describe them as distinct systems. An important aspect of the distinction between these two domains was recognizing the motivational state that follows from neurochemical activity as the outer boundary of the emotion process, a boundary that separates the qualitatively distinct phenomena of emotion and cognition. Because emotion experience has motivational and cue-producing functions and because cognition is often essential in guiding person-environment transactions, the interaction of emotion and cognition is common. Emotion-cognition interactions occur in all the many coping activities that require stimulus appraisal and judgment before action. Such interactions lead to affective-cognitive structures, the frequency and nature of which are limited only by the joint capacities of the emotions and cognitive systems (Izard, 1977 (Izard, ,1992 . However, despite the readiness with which emotion and cognition interact, some emotion-eliciting stimuli (e.g., odors) never form strong links to cognition. Odors produce a range of emotion responses in animals, including humans (Ehrlichman & Bastone, 1992; Moncrieff, 1966 ). Yet, Engen (1987) and others have shown that odors are not processed and stored in memory in a semantically cohesive way but rather in essentially nonverbal terms. "There is no pure recall of odor perceptions using a name as paired associate.. . .The main function of the sense of smell, then, is not to recall odors for cognitive reasons, but to respond to odors actually encountered" (p. 503). Thus, olfaction provides an example of how the brain, specifically the primitive smell-brain, can process and store information in memory in a nonverbal, and perhaps in some cases noncognitive, fashion. Richardson and Zucco (1989) have suggested that memory for odors may be encoded in a rudimentary sensory form, such as sensory traces, and may be processed in a system that is functionally independent of systems of visual images and verbal representations. It may be essentially through noncognitive processes that odor plays a significant role in mother-infant attachment and maternal nurturance of the young of a number of species (see Schneirla, 1965) . Although emotions and cognition are highly interactive and have reciprocal causal relations, there are heuristic advantages in distinguishing between them (Hilgard, 1980; Izard, 1965; Zajonc, 1980) . A principle advantage is a theoretical framework that enables the study of cognition as a distinct independent variable in emotion activation and emotion as an independent variable in emotion-cognition relations. As argued elsewhere, both evolutionary and developmental considerations support the notion that the emotions system preceded the cognitive system in evolution and outpaces it in ontogeny (Izard, 1972; Izard & Malatesta, 1987; Zajonc, 1980) . It is highly adaptive for animals to be able to feel before they think, as in the case where pain elicits withdrawal or pain-induced anger motivates defensive actions. It is equally adaptive for the preverbal infant (as young as 3 weeks) to smile at caregivers and begin establishing attachment bonds that greatly increase the chances of survival. The weight of cross-cultural and developmental data indicates that a number of emotion expressions are innate and universal and emerge before the infant is capable of cognition as defined here (Ekman, Sorenson, & Friesen, 1969; Izard, Huebner, Risser, McGinnes, & Dougherty, 1980; Izard & Malatesta, 1987) . One can argue that these expressions are not necessarily connected to emotion experiences, particularly when emotion experience is defined to include cognition (Lewis & Michalson, 1983) , but with emotion experience as defined in differential emotions theory it is also possible to make a case for innate expression-feeling congruence (Izard & Malatesta, 1987) . That the young infant's smile is accompanied by positive feeling is suggested by the dramatically different expression and behavior that follow pain or restraint and by the fact that young infants' facial expressions are morphologically the same as those of adults (Izard et al., 1980) . The multisystem model of emotion activation is depicted in Figure 2 . The four types of systems that activate emotions are neural, sensorimotor, motivational, and cognitive. All emotion activation processes necessarily involve a neural system, but neural systems can activate emotions independently of the other types of activating systems. In the neural systems, the generation of emotions can be explained in terms of the activity of certain neurotransmitters and brain structures. The involvement of specific neurotransmitters is well established for the complex patterns of emotions involved in depression and anxiety (Redmond, 1985; Whybrow, Akiskal, & McKinney, 1984) . In the sensorimotor systems, emotions are activated by efferent or motor messages, and the process may include afferent feedback from muscle activity, muscle spindles, or cutaneous receptors. In the motivational systems, defined here to include physiological drives and emotions, the sensory processes involved in a drive state, such as pain, activate an emotion. Similarly, an emotion may activate another emotion to which it is innately linked or associated through learning. In the cognitive systems, processes such as appraisal and attribution lead to emotions. Causal explanations of emotions in terms of the different activating systems (e.g., the neural and cognitive) involve not only different levels of analysis but also different mechanisms and processes. In all systems of emotion activation, however, the generation of emotions lies ultimately in the particular substrates involved in the neural evaluation of the affective significance of information. The likelihood that a particular emotion will be activated depends on the pattern of stimulation, the individual's threshold for that emotion, and other individual differences spawned by both genetic and experiential factors. I argue that from an evolutionary-biological perspective, the four types of emotion-activating systems can be viewed as a loosely organized hierarchical system of emotion activators. It is not a rigid hierarchical arrangement, except that processing at the neural (simplest) level is primal and always necessary, and emotion activation through inference or attribution always requires the cognitive (highest level) system. It is hierarchical in a developmental sense, in that the neural and sensorimotor systems participate in emotion activation before some types of motivation (e.g., heterosexual drive) and such motivational processes before some types of cognition (e.g., higher order formal operations and prepositional reasoning). It is a also hierarchical in terms of complexity of information that can be processed at each level. In terms of capacity for independently processing increasingly complex emotion-eliciting information, the hierarchy of activating systems is as follows: neural, sensorimotor, motivational, and cognitive. Neural processes are the only type of activator that is both a necessary and sufficient cause of emotion. Although the sensorimotor and motivational systems can operate independently of cognition, they frequently interact with cognitive processes in activating emotions. In general, the more complex the emotion-eliciting conditions, the more likely the highest order activation system, cognition, will be called into play. The model is placed in context by considering constraints or factors that influence the operation of the four emotion-activating systems. These include individual differences, social factors, and certain stimulus characteristics. Finally, the adaptiveness of hierarchically arranged systems for generating emotions are examined as a feature of the model. Emotion regulation is not a specific focus of this article, but it should be noted that all four types of emotion-activating systems also function as emotion regulatory systems (cf. Izard & Kobak, 1991) . The vast literature on the biochemistry of anxiety and depression (see Thompson, 1988 , for a review) testifies to the efficacy of neural processes (endogenous neurotransmitters and exogenous drugs) to regulate emotions. A considerable body of evidence indicates that emotions are also regulated by sensorimotor processes (see Izard, 1990 , for a review) and by cognitive processes (e.g., Beck, 1976) . Although neural processes are part of all emotion-activating systems, I propose that there are neural systems that can activate emotions independent of cognition and, in some cases, independent of all the other emotion-activating systems. Structures and pathways involved in subcortical and corticolimbic systems of emotion activation were identified in Figure 1 . Aggleton and Mishkin (1986) , Panksepp (1986) , and others have discussed versions of these systems, and LeDoux (1987) has shown that a subcortical pathway can activate emotions independent of the neocortex. Some broad categories of neuroactive agents that can operate on the neural systems to generate emotions are endogenous hormones and neurotransmitters, exogenous drugs, and direct electrical or chemical stimulation of the brain. There are two types of data that suggest that neural processes can lead to emotion without cognitive mediation. The first comes from psychopharmacological research on emotion-related neurotransmitters and psychoactive drugs. The second derives from research on the effects of direct stimulation of brain structures that constitute the neural substrates of emotions. There is wide agreement among neuroscientists who study anxiety and depression that certain hormones and neurotransmitters are involved in the etiology and course of these clinical phenomena (Gray, 1982; Meltzer, Arora, Baber, & Tricou, 1981; Redmond, 1985) . Probably none of them would claim that these chemical substances are the sole cause of these psychological disorders, but they maintain that biochemical factors are significant determinants. Furthermore, there is substantial evidence that the biochemistry of depression has significant genetic determinants (Hill, Wilson, Elston, & Winokur, 1988; Schlesser & Altshuler, 1983) . Although it is recognized that environmental stress and other experiential factors contribute to the etiology of depression Lazarus's (1991) claim that cognition is necessary for the mediation of genetic and biochemical influences on depression seems overinclusive. Although Lazarus and others may be correct in noting that in some cases cognition mediates emotion responses to psychoactive drugs, the evidence suggests that this is not always the case. Cognitive appraisal of drug-induced sensations might well be sufficient to activate emotions, but an appraisal of the sensations simply as negative would not account for the efficacy of some drugs to activate (or alleviate) depression-related emotions and other anxiety-related emotions. Possibly, different drugs recruit different appraisals and hence different emotions, but to confirm this hypothesis it would be necessary to show that the pattern of sensations induced by a depressogenic drug, for example, is logically related to the pattern of appraisals that induce sadness (Izard, 1972) . If one found a pattern of drug-induced sensations that was capable of eliciting a sadness pattern of appraisals, would one not have to consider the possibility that this pattern of sensations was the emotion of sadness? The critical point here is that the weight of the evidence indicates that naturally occurring or experimentally manipulated changes in brain levels of certain biochemical substances can activate emotions or alter emotion experiences without cognitive mediation. The question is not whether neural processes are always, or even typically, the sole mediators of emotions. No one would advocate this extreme position. The evidence reviewed in the next section indicates that neural processes do indeed influence emotion. I suggest that hormones and neurotransmitters affect emotions directly and that the emotions in turn affect cognitive processes. A great deal of evidence has shown that decreased levels of norepinephrine or serotonin are associated with depression (Meltzer et al, 1981; Schildkraut, 1973) . It is difficult to rule out a role for cognition in bringing about these biochemical changes, and in some cases stress and stress-related cognition may be an important factor. However, there is substantial evidence that physiological mechanisms-hormones, diet, sleep -coupled with a genetic predisposition, can trigger changes in brain levels of these neurotransmitters (Whybrow et al., 1984) . Another type of relevant evidence comes from the numerous studies that have shown the capacity of antidepressant drugs to ameliorate depressive mood (for a review, see Thompson, 1988 ). This evidence is far from definitive. Some drugs work better on some types of patients than on others, and all types are generally thought to work better with concomitant psychotherapy. Nevertheless, few students of the biochemistry of depression doubt the efficacy of antidepressant drugs to alter mood. In general, the relations between neurotransmitters and anxiety are nearly as well established as those for neurotransmitters and depression. For anxiety, as in the case of depression, there is still incomplete agreement as to precisely what neural systems are involved, but there is substantial evidence of the efficacy of a number of antianxiety drugs. A number of experts do agree that the noradrenergic system is central in anxiety (Gray, 1982; Lader, 1974; Redmond, 1985) , but some of them acknowledge that other systems may contribute to anxiety directly, or indirectly, by influencing the noradrenergic system. Of particular interest here are a number of experiments on the biochemical induction of anxiety. Although much remains to be learned about the neural mechanisms involved, there can be little doubt that several chemical agents produce anxiety in humans. For example, carbon dioxide, yohimbine, and amphetamine induce anxiety (see Charney & Redmond, 1983 , for a review), and all these agents activate the noradrenergic system (Grant & Redmond, 1982) . Other substances, for example pentylenetrazol, induce anxiety by acting, at least initially, at nonadrenergic sites. Research on the experiential component of depression and anxiety has shown that the key emotions in these phenomena are sadness and fear, respectively (Izard, 1972) . The biochemistry of anxiety and depression undoubtedly relates to their key discrete emotions, but there is the possibility that other emotions involved in anxiety and depressive disorders may complicate the search for underlying neural mechanisms. Nevertheless, the point at issue is whether emotions of any sort can be activated biochemically, and the weight of the evidence suggests that the emotions in anxiety and depression can be induced by chemical agents. Since the early studies of neurosurgical patients by Penfield (1958; Penfield & Jasper, 1954) and Hess (1957) , a number of researchers have reported eliciting various emotions by direct stimulation of the brain. In pioneering investigations that led to a Nobel Prize, Hess stimulated various areas of the diencephalon and observed emotion responses. After a series of such experiments, Hess concluded that direct stimulation of specific neural structures produced four types of emotion responses: somatic motor responses (e.g., facial expression and postural changes), responses mediated by the autonomic nervous system (e.g., changes in cardiac activity and pupillary dilation), a "psychic response" or mental state, and instrumental behavior (e.g., flight or attack). Hess's (1957) experiments and those of later investigators (e.g., Handler, 1982; Flynn, 1967) indicated that the somatic and autonomic responses and the internal state were elicited directly by brain stimulation, independently of information from the environment. Hess inferred that the stimulation elicited a mental state because expressive and autonomic signs emerged independent of external information input, and the instrumental behavior (attack) followed immediately on the animal's perception (biased interpretation) of some environmental object as the enemy. Hess's work implies that the selectivity or bias in the animal's perception and the organization of instrumental behavior into an effective attack was determined by the emotion experience-motivation, action tendency or readiness, cues for perception and cognition, and feeling state. Delgado (1969) described numerous clinical investigations in humans in which electrical stimulation of the brain (ESB) was used for diagnostic or therapeutic purposes. In these cases, ESB 76 CARROLL E. IZARD in different structures produced subjective experiences and behavioral signs of joy or pleasure, anger, and fear. More recent clinical investigations of patients with intractable temporal lobe epilepsy suggest an essential role for the limbic forebrain in the generation of conscious experience, including experiential emotion (Gloor, Olivier, Quesney, Andermann, & Horowitz, 1982) . Gloor et al. observed emotion (and other) experiences resulting from both spontaneous seizures and electrical stimulation that was being used for diagnostic or therapeutic purposes. By monitoring brain activity with depth electroencephalography, they noted that the patients reported experiential phenomena only when the seizure or electrical stimulation affected areas of the limbic forebrain. Seizure activity or electrical stimulation of the amygdala frequently resulted in the patients reporting fear experiences. In a series of ingenious ESB studies in cats, Flynn (1967) not only successfully elicited anger or rage states but also showed that these states and their accompanying expressive manifestations could be elicited independently of aggressive actions. More important, he confirmed Hess's (1957) conclusion that the somatic-expressive and autonomic responses and the presumed accompanying subjective state were centrally controlled, whereas subsequent instrumental or aggressive behavior was controlled by sensory input. With electrodes implanted in the cat's hypothalamus, and in some cases in the amygdala and the hippocampus, Flynn (1967) stimulated free-ranging cats under various environmental conditions. First, he showed that electrical stimulation of the hypothalamus of an otherwise normal cat elicited a display of rage. Second, he found that when various objects, ranging from an anesthetized rat to a styrofoam block, were available, most of the stimulated cats would selectively attack the rat and ratlike objects. Seven of 9 cats in the experiment never attacked the styrofoam block, and only 1 of them attacked the items indiscriminately. Clearly, the animals perceived and appraised the stimuli selectively. It is reasonable to assume that Flynn's work confirms Hess's (1957) inference that the cat's psychic response or emotion experience influenced perceptual and attentional processes and motivated the attack. The instrumental behavior (aggressive attack) was channeled by information from the environment. Of particular relevance to the hypothesis that central neural processes are a sufficient cause of emotion, Flynn (1967) examined the role of the relevant sensory systems (olfaction, touch, and vision) and information input from the environment in the stimulation-emotion-attack sequence. Removal of the olfactory bulb had no effect on the somatic expressive behavior or on aggressive attack. Blindfolding the cats had no effect on the somatic expressive behavior but reduced the frequency of attack from 100% to 40%. Sectioning the mandibular branches of the sensory fibers of the trigeminal (eliminating perioral sensation) had no effect on the somatic expressive behavior but substantially reduced the frequency of attack; in almost half the cats deafferentation completely eliminated attack behavior. When both perioral sensation and vision were blocked, none of the cats exhibited instrumental or attack behavior. Flynn (1967) concluded that the somatic expressive behavior (facial-postural display, sniffing, and walking) was a direct effect of brain stimulation independent of information from the environment. He called Hess's (1957) psychic response, or internal state, a motor disposition, a term equivalent to the action tendency or action-readiness aspects of the present definition of emotion experience. When a range of stimuli are present, this motor disposition plus sensory input lead to selective attack on the appropriate stimulus. Bandler ( 1982) extended the work of Hess (1957) and Flynn (1967) by using microinjections of glutamate, an excitatory amino acid transmitter. The advantage of this procedure is that glutamate affects only the cell bodies at the injection site and not the axons passing through to other areas. Bandler located a population of neurons in midbrain central gray where glutamate elicited the rage display and, when adequate stimuli were present, aggressive attack. Basically, he reaffirmed the conclusion of Hess and Flynn. He concluded that the glutamate activated central processes that elicited rage expressive behavior independent of cognitive processes based on environmental information. Like the earlier investigators, he saw sensory input from the environment as the information that guided the attack behavior. He rejected Hess's concept of an elicited psychic response, describing the attack motivation "as a product of level setting in sensory and motor systems" (Bandler, 1982, p. 390). This notion of altered thresholds for sensorimotor responses may be related to the action readiness or action tendency component of the present definition of emotion experience. Although the terminology differs across investigators, the conclusion is essentially the same. All agree that direct stimulation of neural substrates of emotion produce emotion expressive behavior, ANS activity, and some kind of motivational, experiential state independent of environmental information. Conceivably, the set of responses to direct stimulation might vary across different emotions. The investigators also agree that it is the sensory input from the environment that guides the emotion-related instrumental or goal-directed behavior. It is the transformation and integration of the environmental information necessary to the attack, escape, or other emotion-related behavior that requires higher order cognitive processes. In a series of experiments, Zajonc and his colleagues found that changes in subjective states of pleasantness or unpleasantness could be induced by expressive and nonexpressive facial muscle contractions that altered cerebral blood flow, the blood-cooling capacity of the cavernous sinus, cerebral blood temperature, and, presumably, subsequent neurochemical processes that mediate subjective feelings. Although the first statement of this emotion activation model (Zajonc, 1985) was challenged on evolutionary and neurological grounds (Burdett, 1985; Fridlund & Gilbert, 1985; Izard, 1985) , Zajonc has modified his position, and his experimental findings have not been challenged by other investigators. A series of experiments by LeDoux and his colleagues (LeDoux, 1987 (LeDoux, ,1989 has demonstrated that acoustically and visually conditioned fear can be established in rats after the FOUR SYSTEMS FOR EMOTION ACTIVATION 77 acoustic or visual cortex, respectively, has been ablated. LeDoux identified subcortical structures that mediated the conditioned fear response. The circuit consists of interoceptors or exteroceptors, thalamic nuclei, and amygdaloid nuclei. The relatively small number of synapses in this thalamoamygdaloid pathway makes transmission very rapid and enables an animal to make an immediate response. This mode of responding is highly adaptive when information-processing demands are simple and the animal has to respond rapidly to the broad physical features of the stimulus. When the situation requires more complex evaluation, processing occurs in a thalamo-corticoamygdaloid pathway. LeDoux (1987 LeDoux ( ,1989 concluded that the amygdala is the key structure for the immediate evaluation of the emotional significance of stimuli and the releasing of emotion responses. It is involved in both the subcortical and the cortico-limbic pathways. LeDoux inferred that these dual pathways for emotion activation constitute separate systems for affective and cognitive information processing. Although LeDoux's evidence does not provide direct support for the idea that neural processes are sufficient causes of emotion, it does indicate that neural-evaluative processes lead to emotion without higher order cognition or cognition that requires cortical processing. Since the beginnings of the scientific study of emotions, theorists have recognized a relation between the motor system and subjective states. Darwin (1872 Darwin ( /1965 observed that "the free expression by outward signs of an emotion intensifies it" (p. 365), and James (1890/1950) said, "Refuse to express a passion and it dies" (p. 463). Whereas these statements suggest only that sensorimotor processes can regulate ongoing emotion experiences, James attributed even greater powers to expressive behavior. He indicated that the quality of feeling states could be altered from undesirable to desirable if "we . . . assiduously . . . go through the outward movements of those contrary dispositions which we wish to cultivate" (James, 1890 (James, /1950 . In these statements, the effect of expressive behavior is confounded with that of intention and cognitive self-instruction. However, Darwin's and James's view on the role of somatic responses in emotion experiences is not inconsistent with the data showing that the motor system responds to direct stimulation of emotion substrates (Bandler, 1982). Of the various aspects of the sensorimotor-activating systems, facial expression and posture have been studied empirically. The sensorimotor processes are as follows:  A number of theorists have extended the thinking of Darwin (1872 Darwin ( /1965 and James (1890 James ( /1950 and postulated that sensory feedback from facial and postural movement is a sufficient, though not a necessary, cause of emotion experience (Izard, 1971; Tomkins, 1962) . Laird (1974 Laird ( , 1984 ) went a step further and proposed that experimenter-manipulated emotion expression can generate emotion experiences, and some investigators suggested that such emotion activation is independent of cognitive processes. Theories in the tradition of Darwin and James and the hypothesis of Laird (1974 Laird ( ,1984 have led to about 30 published studies on facial feedback as a determinant of subjective states of emotion. These include several critical reviews and metaanalyses of the empirical studies (Adelmann & Zajonc, 1989; Izard, 1990; Matsumoto, 1987; Winton, 1986) . The various forms of the hypotheses suggest that expressive behavior can (a) alter ongoing emotion experience, (b) generate positive or negative emotion experiences, and (c) activate a specific emotion experience corresponding to the manipulated expression. There is a substantial body of evidence supporting the first and second forms of the facial feedback hypothesis and some favoring the third form, the notion that expressive behavior can activate emotion-specific experiences (e.g., Ducios et al., 1989). Consistent with the Ducios et al. finding of the specificity of expression generated experiences, Ekman, Levenson, and Friesen (1983) reported that experimenter-directed facial action produced emotion-specific patterns of ANS activity. Furthermore, in a follow-up study, Levenson, Ekman, and Friesen (1990) found that directed facial action elicited emotion-specific patterns of ANS activity and specific subjective experiences without the subjects seeing their faces in a mirror or the face of a model. The data from the Levenson et al. replication did not appear quite as robust as that of the original study, and emotion-specific ANS patterns from directed facial action have not yet been reported from other laboratories. Although the effects of expressive-behavior manipulations on emotion experience have been replicated many times, some skepticism remains as to whether the relevant experiments have completely controlled for cognitive influences . However, Zajonc et al. used procedures that seem to eliminate cognitive influences, and they reported that facial muscle contractions generated pleasant or unpleasant feelings by increasing or decreasing cerebral blood flow and thereby decreasing or increasing brain-blood temperature and neurochemical activity. Both Darwin and James included posture when they described the effects of expressive behavior on emotion experience. James (1932) was quite specific. He described the posture of expansion-erect head and trunk, expanded chest, and raised shoulders-as associated with positive states like pride and self-esteem as well as negative states like contempt. He described the posture of contraction, forward trunk, bowed head, and drooping shoulders, as characteristic of states of sadness, depression, and abasement. In the tradition of Darwin and James, Bull (1951) proposed a motor-attitude theory of emotion activation. In her model, the sequence is as follows: Stimulus -*• neural organization -»• bodily readiness, action set (motor attitude) -»• oriented feeling or mental attitude -*• action. For Bull, the motor attitude is the proximal cause of a feeling state or "oriented awareness." 78 CARROLL E. IZARD Despite the observations of Darwin (1872 ), James (1932 ), and Bull (1951 , only a few empirical studies have examined the effects of posture in emotion. In a longitudinal study, Weisfeld and Beresford (1982) showed that boys, ranked by peers in early grade school as tough or dominant, were characterized by erect posture in high school. In another study, they found that erectness of posture in college students on receiving the results of a test was positively correlated with their test performance. Although the foregoing findings suggest only a correlation between posture and mood, Riskind and Gotay (1982) and Riskind (1984) showed that manipulations similar to James's (1932) expansion and contraction postures altered emotion experiences, expectations, and task persistence in the expected directions. In a series of three studies, Riskind (1984) showed that the appropriateness of the posture to the situation influenced the effects of the posture. For example, a slumping posture increased ongoing sadness or discouragement, but it also helped the person to recover from the discouragement more quickly. Riskind concluded that appropriateness of posture or posture-mood congruence enhanced the person's effectiveness in coping with both rewarding and stressful situations. Because Riskind's (1984) studies always involved the posture manipulation in interaction with a success-failure manipulation, he did not show that posture alone activated emotion experience. The studies did show, however, that posture could have an effect seemingly independent of, and contrary to, cognitive influences, as in the case of an induced (and inappropriate) slumping posture having an adverse effect following a success experience. In the study demonstrating the emotion-specific effects of facial expressions, Duclos et al. (1989) examined the direct effects of emotion-specific postures corresponding to sadness, anger, and fear. The selection of movements for encoding the postures was guided by descriptions in emotion theories. After assuming a given posture for 15 s, subjects rated their feelings on the target emotion and seven others. The results showed that the postures of sadness, anger, and fear elicited the highest ratings for feelings of sadness, anger, and fear, respectively. The authors concluded that emotion postures had clear and specific effects on emotion feelings.
Velásquez developed a comprehensive architecture of emotion based on Izard's four systems model REF , focusing on the neural mechanism underlying emotional processing.
Four Systems for Emotion Activation: Cognitive and Noncognitive Processes
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