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Web Topic 10.4
Emotion, Drive, and Motivation

Introduction

Motivation theories attempt to explain how and why animals perform different behaviors at different times. The key principle underlying this book is that animals must continually make decisions about what activity to pursue given the variable nature of the social and ecological environment in time and space. This problem is particularly relevant for mobile animals, and in fact a centralized brain and conscious awareness of the environment are argued to have evolved as a consequence of the “liability” of mobility and the need to make constant decisions (Merker 2005). In this Web Topic unit we briefly review the development of motivation theories. Early models were not construed in ways that were readily testable by physiologists, but subsequent models steadily improved to enable such tests. Emotional constructs became embedded in this motivational framework. In some cases, emotions and motivation are signaled to receivers, or receivers may detect inadvertent cues from behaving individuals that reveal information about their motivational or emotional state. We therefore conclude this unit by discussing the relevance of these theories to the evolution of honest signaling.

“Drive” models of motivation

The first generation of motivational models viewed motivation as part of a homeostatic drive mechanism that energizes animals, pushing them to rectify physiological imbalances and thus satisfy their internal needs. Homeostasis, the tendency of a system to remain at a stable equilibrium, requires a regulatory system that maintains the animal’s physiological state at an optimal set point. If the physiological state moves off the set point, an error-detection mechanism triggers corrective responses to bring the animal back to the set point, like a thermostat (Cannon 1932; Hull 1943). The need to correct the imbalance generates the drive energy. This drive causes animals to respond to those stimuli that will satisfy the need and reduce the imbalance. Appropriate stimuli for the specific drive are learned and refined with experience, according to the response-reinforcement learning paradigm. In this view, response motor patterns that best meet the animal’s needs in a particular stimulus situation are selectively strengthened through reward reinforcement. Hunger and thirst drives seemed to fit this model well. If a deficit in nutrition or water is detected in the body, physiological mechanisms such as low blood glucose levels or body fluid levels initiate and direct food- or water-seeking behaviors. Once found, the animal consumes or drinks until the system set point is restored and the drive is reduced. Evolutionarily built-in goals, such as reproducing (sex drive) or chasing off a threatening rival (aggression drive), were similarly viewed as motivating set points from this homeostatic perspective. These ideas prompted researchers to search for the physiological set points and the deficit signals in the brain (Pfaff 1982). However, numerous problems emerged. First, set points appeared to be highly flexible and variable and thus not very stable (Bolles 1980). This observation lead to the alternative concept of settling points, a stable state caused by a balance of opposing forces, which gives the illusion of a set point but without the homeostatic mechanisms (Wirtshafter and Davis 1977). Second, an animal’s behavior could be strongly affected by anticipation of a goal, by social effects, and by availability of resources; in other words, other cognitive and external factors needed to be considered (Weingarten 1983; Schulkin 2003). Third, the homeostatic mechanism of drive reduction upon fulfilling the physiological need could not be demonstrated, even for hunger and thirst drives. For example, intraveneous feeding or introducing food directly into the stomach does not stop an animal or human from consuming more food (Miller and Kessen 1952; Turner et al. 1975).

Another early model was the hydraulic model of motivational drive by the ethologist Konrad Lorenz (Lorenz and Leyhausen 1973), which attempted to explain why the level of motivation builds up as a function of the time since the last reward. This model uses the metaphor of the flush toilet (Figure 1). Drive grows internally like the build-up of pressure in a fluid reservoir, which at some point bursts through an outlet. Proposed internal sources of the build-up could be physiological depletion cues or secreted hormones related to hunger, thirst, aggression, and sex. The model also incorporates the presence of external stimuli that can increase the probability of triggering the motivated behavior. An external stimulus is more likely to trigger the behavior if the drive pressure is high than when it is low. If the drive pressure is very high, it might burst through the outflow even with no external stimulus, called a vacuum response. This model was thus put forward as a way to explain the spontaneous occurrence of behavioral acts by animals that have been prevented from performing their normal behaviors. Although this model was not readily adopted by neuroscientists because it didn’t offer useful details of neural mechanisms, it did deal with the interaction between internal motivating factors and external stimuli in controlling behavior, and offered an explanation of the phenomenon of spontaneous acts by thwarted animals. Hogan (1997, 2005) developed a similar model of motivation around the concept of energy as a way to overcome some of the shortcomings of Lorenz’s model. He envisioned an energy variable that has multiple sources of internal and external input energy, and multiple means of dissipating the energy. This model still requires a threshold variable that specifies when the behavior is likely to occur.

The drive models explain some properties of motivated behaviors, such as the increase in goal-seeking behavior as a function of time since the last reward, the ability of animals to learn appropriate responses in a given stimulus situation, and the occasional examples of spillover behaviors, but they fail to provide a physiologically-based answer to the mysterious source of the driving energy, and don’t address the frequent observation of behavioral flexibility of responses by animals. Although they posit separate drive systems for different types of motivated behaviors, these models also don’t address the common observation of interactions between different drives, such as motivational conflict described in Chapter 10 of the main text (Berridge 2004; Anselme 2010).

Figure 1: Hydraulic drive model of motivation. Fluid enters a reservoir through the tap, which represents a continuing flow of energy from endogenous sources. The height of the fluid in the reservoir indicates the build-up of drive energy. The fluid is held in the reservoir by a spring-loaded valve, which represents the inhibitory pressure from higher-level brain areas. The weighted scale pan represents the strength of external releasing factors, which can increase the likelihood of valve release in addition to the pressure from the fluid in the reservoir. When the valve opens, energy flows through the outlet into a slanted trough. The holes on the bottom of the trough coordinate muscle action pattern responses, where the yellow numbers indicate the rank of the response strength. (After Lorenz 1950.)

“Incentive” models of motivation

In contrast to the energy-driven and drive-reduction models for behavioral decision making, incentive motivation models envision motivation as a mental state responsible for changing an animal’s receptiveness to specific environmental stimuli (Berridge 2004; Anselme 2010). The first step in the development of these ideas was the discovery that hungry rats would suddenly change their behavior when offered tasty (sweet) but nutritionless rewards (Pfaffmann 1960). Pleasurable sensations (called hedonic rewards) appeared to be motivating factors by themselves, even in the absence of a drive-reduction effect. Pleasurable sexual sensation, even the anticipation of it, was also found to be a powerful motivating force (Sheffield 1966). Thus affective reactions (i.e., emotions) such as liking, disliking, fear, and anger became more explicitly incorporated into this second generation of motivational models. Bolles proposed that animals were motivated by the learned expectation of hedonic reward, not by internal deficit states (Bolles 1972). Bindra then clearly laid out the alternate learning paradigm implicit in this view (1974, 1978). Rather than learn a specific motor pattern in response to a given rewarding (or aversive) stimulus, an animal’s response is dependent on what it perceives at the time of stimulus presentation. Via learning and experience, animals develop cognitive representations of correlated sets of environmental stimuli that characterize particular goals or incentive objects. The suite of stimulus characteristics representing these goals or objects then becomes strongly associated with the hedonic reward they provide. The objects thereby acquire an incentive salience value. Response acts are flexibly determined at the moment as a function of the animal’s current internal condition, motivational state, and sensory inflow from both within the body and from the environment. In contrast to the drive models, a physiological deficit does not drive the seeking behavior directly, but can magnify the hedonic impact and incentive salience of the object or conditioned stimulus associated with the goal (Toates 1986). Motivational states thus stimulate perception and focus attention on key eliciting stimuli in a given context so that the animal performs the appropriate set of behavioral acts to achieve its goals. These kinds of models account for observed flexibility by animals far better than the response-reinforcement associations postulated by the drive models. For example, animals often perform different responses to the same stimulus situation that nevertheless achieve the same goal. An animal may take advantage of a feeding or drinking opportunity, even though it is not particularly hungry or thirsty, because it is uncertain when such opportunities will occur next. And animals perform nuanced behaviors in response to complex social stimuli such as a rival or potential mate.

Incentive models predict that neural pathways for motivational resolution in the brain’s limbic area must project to higher brain areas responsible for sensory-perception integration of external stimuli, and not directly to motor areas as predicted by the drive models. Brain circuits and nuclei that fired in response to hedonic stimuli were soon discovered (Stellar 1982), and a new field called affective neuroscience emerged (Davidson and Sutton 1995; Panksepp 1998; Rolls 1999; Davidson et al. 2000; LeDoux and Phelps 2000). The search for drive-dedicated neurons initially found no evidence that specific motivations or emotions were restricted to specific neurons. Rather, stimulation of key regions of the forebrain basal ganglia and limbic system nuclei (hypothalamus, hippocampus, amygdala, ventral tegmentum, nucleus accumbens, and ventral pallidum) evokes a range of motivated behaviors and both positive and negative emotions. These brain regions are connected by circuits and feedback loops of neurons with different types of neurotransmitters that have excitatory, inhibitory, and disinhibitory effects (Figure 2). The mesolimbic dopamine system seems to be responsible for the arousal of non-specific “wanting” (Gray et al. 1999). Dopaminergic neurons originate in the ventral tegmentum of the basal forebrain and send projections to the hippocampus, amygdala, nucleus accumbens, and prefrontal cortex. Stimulation of the nucleus accumbens in particular initiates seeking or exploratory behavior (Reynolds and Berridge 2002). The prefrontal cortex is the site of executive function, where attention is focused on features of preferred stimuli and decision making is accomplished. Activation of the dopamine system then stimulates the release of the neurotransmitter acetylcholine by cholinergic neurons throughout the brain; acetylcholine facilitates the integration of sensory input in the cortex, and also operates at neuromuscular junctions in the brain stem to cause approach and retreat actions. GABAergic neurons send inhibitory signals among the ventral tegmentum, ventral pallidum, and specific areas within the core shell of the nucleus accumbens, and appear to play a major role in activating “liking” responses and positive emotional expressions (Berridge 2003). Complex feedback loops with other types of neurons may then disinhibit these inhibitory effects. Although these circuits and brain regions do not encode specific motivational systems, some evidence is accumulating for the existence of dedicated neuropeptide transmitters for some motivational functions. The hypothalamus appears to possess neurons containing dedicated hunger peptides (e.g., leptin, neuropeptide Y, cholecystokinin, ghrelin) and specific receptors for these peptides. Thirst may be regulated by brain receptors for another neuropeptide called angiotensin II. Endogenous opioid-peptides (e.g., endorphins, enkephalins, dynorphins, and endomorphins) play an important role in mediating positive emotions, liking, and reward-seeking. In the section below on emotions, we summarize the brain circuits involved in these and other motivational systems. The point here is that different forebrain circuits combine with cortical visual, auditory, and olfactory input in the prefrontal cortex to enable animals to take appropriate goal-directed actions, as predicted by the incentive models.

Figure 2: Brain areas involved in motivation and emotion. Sagittal section through a rat brain showing key nuclei in the limbic system. Main neuronal circuits for mesolimbic dopamine system, showing dopamine neurons ascending from ventral tegmentum (red), glutaminergic pathways (blue) linking prefrontal cortex, hippocampus, and basal ganglia, and GABAergic inhibitory neurons (green). Green boxes show key nodes in this system. Other nuclei and brain areas discussed in this web topic unit are also shown. Abbreviations: PAG = periaqueductal gray area; DR = dorsal raphe nucleus; BST = bed nucleus of the stria terminalis. (After Kelley and Berridge 2002; Berridge 2004.)

The next-generation incentive model, called the uncertainty processing theory (UPT), attempts to address three problems with the earlier incentive models: 1) how motivational state actually affects behavior and cognitive processing, 2) how motivational specificity can be achieved, and 3) how interactions and conflicts among different motivational systems are resolved. The UPT argues that motivation is the brain’s solution to the problem of environmental uncertainty about psychologically significant events (Anselme 2010). Motivation is proposed to operate like an information processing center that enables animals to acquire knowledge about the contexts in which important events are likely to occur, highlight such events or their stimulus features as incentive objects, and reduce uncertainty about them through the recruitment of anticipatory and attentional cognitive activity. The model, shown in Figure 3, is derived directly from current knowledge of motivational processing in the brain.

Figure 3. The uncertainty processing theory of motivation. The flow diagram shows neurotransmitter pathways to the anticipation processing center (yellow) and the attention processing center (light blue); type of neurotransmitter indicated in blue. An event important to the animal’s fitness is indicated by the red box. The animal’s psychological state of uncertainty about this event is represented by the orange box. The probability PE of an event occurring ranges from 0 to 1; uncertainty is highest at PE = 0.5; certainty is high if the event is either very likely to occur (PE = 1) or very unlikely to occur (PE = 0). Prior experience and knowledge of this event (purple) reinforces the incentive salience value (positive or negative valence) for this event. Excitatory and inhibitory connections among the basal ganglia, together with decisions in the prefrontal cortex, determine the type of motivation elicited by the event and initiate seeking behavior. Approach or avoidance depends on the direction of reinforcement in earlier encounters with the event. (After Anselme 2010.)

High uncertainty about especially salient events such as food items, mates, rivals, or predators, could imperil reproduction and survival, so striving to reduce uncertainty about both liked and disliked events is strongly favored by natural selection. Uncertainty is proposed to be the factor that releases motivated behaviors in changing environments. As mentioned earlier, mesolimbic dopamine plays a key role in causing reward expectation and wanting. The UPT goes one step further by suggesting that dopamine encodes uncertainty for a wide range of positive and negative events. Key evidence for this assertion derives from a study showing that activation of dopamine neurons peaks when the probability of receiving a reward is 0.5, and gradually diminishes as reward probability becomes more predictable (i.e., approaches 0 or 1) (Fiorillo et al. 2003). Moreover, dopamine neurons are more responsive to the anticipation of rewards rather than to the receipt of a reward, and to novel attention-grabbing stimuli (Schultz 1998, 2002). Dopamine projections to the prefrontal cortex, basolateral amygdala, and hippocampus are involved in anticipation of a reward. These areas in turn interact using glutamate and converge their projections onto the nucleus accumbens, which processes anticipation and facilitates flexible approach responses via indirect connections to motor neurons (Ikemoto and Panksepp 1999). In the next step, motivational specificity occurs via a selective attention process. Cholinergic neurons (acetylcholine) originating in the basal forebrain project to cortical regions of the brain and are involved in discrimination and processing of sensory information from all modalities. When an animal in a given physiological state (e.g., deprived) has the opportunity to establish physical contact with a useful object for that context (e.g., food), the object acquires psychological significance as a consequence of its hedonic value, which can then be represented mentally. The learned association between physiological state and the object’s value establishes a goal and modulates the seeking behavior. The response may be approach or withdrawal depending on whether the direction of reinforcement during prior encounters was positive or negative.

The UPT model offers a possible explanation for the behaviors animals perform when confronted with two conflicting events, as we described in the section on motivational conflict in Chapter 10 of the main text. Animals and humans presented with two types of salient stimuli show ambivalence, delayed reaction times, and increased error rates; if the responses are truly incompatible, one type of response eventually prevails while the other is inhibited (Figure 4A). This could be caused by the limited ability of the brain to attend to two different events at the same time, given the common pathway for anticipation and selective attention. The activation of the dopamine-cholinergic pathway for one event means that it is less available to deal with another event; the attention and response thresholds for this event are therefore raised (Figure 4B; see also main text Figure 10.7). If two events are both strong stimuli, they may each mutually inhibit the other as a consequence of attentional interference (Anselme 2010).

Figure 4: Attentional interference during motivational conflict. Two motivational causal factors are shown in both graphs with numbers indicating the different factors (e.g., thirst and hunger, or fear and anger). The attentional threshold is shown by the bar labeled A(1 or 2) and the higher response threshold by R(1 or 2); the bracketed M region indicates the motivational strength for the respective factor. (A) When only one motivational causal factor is stimulated to a level above its attentional and response thresholds, the attention and response thresholds for the other causal factor are raised (dashed arrows). The animal focuses it attention only on the strongly motivated stimulus and performs the appropriate response behavior, while attention and behaviors appropriate for the other causal factors are inhibited. (B) If two causal factors are both simultaneously stimulated, each raises the thresholds for the other one, but if the intensities of both stimuli are above their thresholds, the consequence is attentional interference (tan arrows), which in this case is stronger for M1 compared to M2. (After Anselme 2010.)

Whether or not dopamine turns out to encode event uncertainty, it clearly does instigate an urge to adopt resource-seeking behaviors such as approach, exploration, and investigation. In humans, dopamine injection causes euphoria. Which leads us to a discussion of the role of emotions in motivating behavior.

Emotions

Emotions are an important component of motivational systems. As discussed above, wanting is a dopamine-dependent process that makes animals more receptive to certain stimuli and transforms them into desired goals—the incentive salience component of motivation. The wanting system probably evolved early in vertebrate evolution to mediate the innate pursuit of key objects such as food and mates and the avoidance of stimuli associated with predators. Although desired goals are usually liked goals (and dangerous objects are fear-inducing objects), liking and disliking represent distinct hedonic (emotional) processes compared to wanting, and liking and wanting are facilitated by different neurotransmitters and neural circuits. Expressions of hedonic pleasure or displeasure and associated neurological changes occur upon consumption of a reward (e.g., tasty food versus bitter food). Such emotions operate as reinforcers during the process of learning the incentive value of various environmental stimuli (Cardinal et al. 2002; Berridge and Robinson 2003). Within the construct of motivation, the feelings generated by hard-wired emotional systems facilitate the acquisition of environmental knowledge and skill. In the broader view, different emotions stimulate organisms to respond quickly to external events in ways that optimize fitness (Darwin 1872).

Emotion is an umbrella term that includes affect (feelings), along with cognitive, behavioral, communicative, and physiological manifestations. Emotions are triggered by external events and often lead to rapid onset and short duration effects, in contrast to moods, which are brought on by less obvious antecedents and have longer lasting effects. Most mammals possess a core set of emotions—seeking, fear, anger, play, panic, lust, and care (Panksepp 2005). Birds and other vertebrates also show many of these emotional behaviors. Evidence for these core emotional systems includes the ability to elicit specific response behaviors by stimulating key subcortical brain nuclei (Panksepp 2003a), and in human fMRI studies the activation of different brain regions by individuals experiencing different emotions (Damasio et al. 2000; Phan et al. 2002). In humans, emotional responses occur on two levels: a subconscious level that involves subcortical pathways, the autonomic system, and involuntary behaviors and facial expressions; and a conscious level that directs the behaviors to appropriate targets and modulates some of the involuntary expressions. We don’t know the extent of animals’ cognitive experiences during emotional episodes but we do see evidence of the physiological effects, communicative expressions, and directed responses. Rats and monkeys will eagerly press levers to obtain an injected dose of heroin, a plant-derived opiate that mimics the pleasurable effects of endogenous opioids found in all mammalian species. Below is a brief overview of the core emotional systems. Each one is based on a different brain circuit that links basal ganglia, thalamus, and a distinct portion of the frontal lobe (Alexander and Crutcher 1990).

The seeking system is the generalized activation system recruited by all vertebrates to organize the pursuit of food, mates, and shelters. The energizing (wanting) component is driven by the dopaminergic-cholinergic pathway described earlier. Activation of the ventral tegmental area and nucleus accumbens plays a critical role in causing both approach and aversive action responses (Ikemoto and Panksepp 1999; Ikemoto 2007; Zellner and Ranaldi 2010). The hedonic (liking) component is caused by opioid neurons in the nucleus accumbens shell, ventral pallidum and brainstem. These neurons synthesize endogenous opioid peptide transmitters such as endorphins and enkephalins, as well as the specialized G protein receptors for these neurotransmitters. Stimulation or activation of these regions is responsible for the pleasurable sensations that occur once a tasty food item has been consumed (Berridge 2003). In rats, primates, and human infants, the sensation of sweet taste (from taste bud sensors) triggers a characteristic tongue-protruding response, while bitter taste triggers gaping (or the disgust facial expression in older humans). The wanting and liking circuits of the seeking system can be separately knocked out without destroying the other component. Together, the pleasurable experience of an object reinforces the subsequent motivated pursuit of similar objects. A good communication-related example of this seeking and rewarding system has been described in songbirds, where distinct patterns of dopamine activity influence the motivation to produce song, and opioids released as part of social interactions induce further singing (Riters 2011).

The fear system prepares an animal to take appropriate rapid actions in dangerous contexts. It has a dedicated circuit of excitatory (acetylcholinergic and epinephrinergic) neurons. The neural response is initiated in the lateral and central amygdala upon sensory detection of learned or innate cue features. The amydgala plays a key role in distinguishing between aversive and positive stimuli (Etkin et al. 2006; Tye and Janak 2007; Shabel and Janak 2009; Bermudez and Schultz 2010; Morrison and Salzman 2010; Tye et al. 2011). If the stimulus is deemed dangerous, a cascade of involuntary responses is mediated by nerve projections to the anterior and medial hypothalamus, on to the periaqueductal gray area (PAG) of the midbrain, and then to the lower brain stem and spinal cord (Panksepp 2004). This circuitry stimulates the sympathetic nervous system (a component of the autonomic nervous system) and triggers the release of the hormone epinephrine (also called adrenaline) from the adrenal gland, which targets various organs and causes an increase in heart rate, blood pressure and perspiration while inhibiting other non-essential body functions. The behavioral response to stimulation of these specific subcortical brain areas is freezing, startling, or fleeing; cognition may be involved in assessing which of several alternative escape behaviors is best given the current conditions. This emotion is sometimes accompanied by a scream vocalization, and in humans by a fearful facial expression.

The context and function of the remaining core emotions is the mediation of social interactions. The anger system shares some circuits with the fear system. The orbital frontal cortex first processes sensory input from social cues and signals, typically olfactory in the case of rodents and visual and vocal in the case of primates. Neural pathways then descend to the medial amygdala, which, as in the fear system, evaluates whether the stimulus is aversive or positive. Pathways then extend to several areas in the hypothalamus, thalamus, lateral septum, and bed nucleus of the stria terminalis. These centers send projections to the periaqueductal gray area and the lower brain stem, as in the fear system. The hypothalamus also connects directly to the pituitary gland, which releases various hormones directly into the body’s circulatory system that target the adrenal gland. Noradrenaline (norepinepherine) plays an important role in aggression as both a neurotransmitter in the brain and as a circulatory hormone produced by the adrenal gland. As in the fear response, these hormones increase heart rate and blood supply to the muscles and prepare an animal to fight if necessary. Various aggressive signals, facial expressions, and postures are involuntarily produced from the output of these subcortical ganglia. In addition, neural pathways from the subcortical ganglia ascend through the thalamus into the cortex to permit some voluntary control and assessment of the anger-evoking stimulus. The dopamine motivational circuit must be intact in order for animals to display the full aggressive behavioral repertoire toward a rival individual. Finally, steroid hormones such as testosterone and estrogen are also necessary to sustain aggressive behavior. Testosterone seems to primarily have an organizational effect on the brain, especially in males, by making aggression-inducing stimuli more salient; testosterone affects responsiveness in the lateral septum, amygdala, and dorsal raphe nucleus. Testosterone also promotes the development of aggressive behavioral skills through play behavior in young mammals (Nelson and Trainor 2007).

The play system also seems to have its own set of circuits, although they overlap with circuits for other emotions. Play behavior is the first type of non-mother-directed social interaction in a young mammal’s life. It provides a crucial opportunity for learning adult social skills, practicing aggressive behaviors, establishing one’s position in the dominance hierarchy of peers, and discriminating the sexes, and natural selection has imbued it with a pleasurable motivating reward system. The opioid and dopamine reward circuits are recruited to motivate play behavior. Cholinergic, noradrenergic, and opioid neuron circuits underlie the attentional processes needed for focusing on the rapidly performed actions and learning from errors. The cortex is not involved in play initiation, but it does affect play performance, in the sense that decorticated animals are hyperactive and very aggressive. Built-in mechanisms thus inhibit lethal acts during play. Playing animals also spontaneously give characteristic playful vocalizations. As mentioned above, testosterone is involved: males are more likely to initiate play and respond to play initiation signals by other males (Siviy and Panksepp 1987a, b; Panksepp et al. 1994; Vanderschuren et al. 1997; Knutson et al. 1998).

The panic system operates primarily in young mammals that have been separated from the parent, and elicits vocalizations of pain, distress, and crying. This behavior appears to be initiated in a region of the cortex called the anterior cingulate. Stimulation of this area leads to activation of the bed nucleus of the stria terminalis, the ventral septal and dorsal preoptic areas, and then on to the dorsomedial thalamus and the periaqueductal gray area of the brain stem. This circuit is called the thalamo-cingulate limbic pathway (Herman and Panksepp 1981; Panksepp 2003b; Newman 2007; Panksepp and Watt 2011). No learning is involved in this pathway, as it occurs in very young infants after being isolated. The effects can be modulated and diminished by the application of various opioid peptides, oxytocin, and the monoamine neurotransmitter serotonin.

Feelings of social attachment and bonding in mammals (care and lust systems) are facilitated by release of oxytocin and vasopressin, often called love hormones (Nelson and Panksepp 1998). These peptides are synthesized by specialized cells in the paraventricular nucleus of the hypothalamus. Some of these cells extend projections into other parts of the brain, such as the prefrontal cortex, basal ganglia (amygdala, ventromedial hypothalamus, septum, nucleus accumbens), and brain stem (Morgane et al. 2005), where they operate as neurotransmitters. Receptors for these neurotransmitters are also synthesized in these brain regions. Other cells in the hypothalamus send projections to the nearby pituitary gland, which stores oxytocin and vasopressin and releases these chemicals into the blood stream, where they operate as hormones. They target various organs involved in reproduction, including mammary glands and uterus in females and gonads in both sexes. Since these peptides are too large to pass the blood–brain barrier, their joint physiological and psychological effects are believed to be coordinated by synchronous release into the brain and circulatory system. Oxytocin is particularly important in female mammals. It increases immediately after birth and regulates aspects of bonding with infants (Nowak et al. 2007). A large surge of oxytocin occurs during sexual behavior and orgasm. In monogamous mammals such as the prairie vole (Microtus ochrogaster), administration of central oxytocin induces pair bond formation and greater social contact; this species has many more oxytocin receptors than closely related rodents with polygamous, non-pair-bond social systems (Williams et al. 1994). Vasopressin is chemically similar to oxytocin and plays a role in facilitating paternal care in male mammals. Some other neurotransmitters also facilitate positive social interactions. Endogenous opioids are rewarding and can induce odor and place preferences; they are also released during bouts of affiliative interaction such as suckling, physical contact, allogrooming, and social play. Opioids are postulated to encourage animals to engage in affiliative social behaviors by inducing a euphoric state (Nelson and Panksepp 1998). The opioid reward system also plays an important role in reinforcing sexual behavior in male mammals (Agmo and Berenfeld 1990).

An important message to be extracted from these summaries of the neurophysiological bases of emotional systems is that each is associated with diagnostic expressions—in other words, communication signals. Food-seeking is associated with expressions of liking, such as smiles and tongue extrusion, and expressions of disliking such as gaping and disgust facial expressions. Fear is associated with screams and fearful expressions; anger with aggressive postures, staring, weapon presentation, and mouth expressions; and panic with cries and expressions of pain and sadness. Care and lust systems are associated with physical contact gestures and smiles; and the play system is associated with invitation postures, play faces, and laughter. For the most part, these expressions occur involuntarily based on subcortical neural pathways to various motor systems; they can occur in animals with a non-functional cortex. They are therefore honest indicators of the emotional feelings the sender is experiencing. The signals have evolved for this purpose because of direct social benefits to senders and costs of cheating. Nevertheless, they can often be modulated and controlled voluntarily to some degree because of cortical loops in all of the systems. This issue is discussed in detail for human emotional expressions in Chapter 16.

A final point is the inevitable urge by biologists and psychologists to categorize emotions, especially in humans, because we have many more described emotions than animals do. Early attempts by several researchers converged on a two-dimensional model, in which emotions are placed on a grid or circle with two orthogonal axes, one representing level of pleasantness (e.g., positive versus negative feelings, or valence), and another axis representing arousal level (high versus low) (Russell 1980; Watson and Tellegen 1985; Thayer 1986; Russell et al. 1989; Larsen and Diener 1992; Yik et al. 1999). Figure 5 shows a melded version of these models.

Figure 5: Two dimensional circumplex model of emotions. The vertical axis is arousal level, and the horizontal level is pleasantness. Various emotions can be organized around the circle based on combinations of these two axes. (After Yik et al. 1999.)

This type of model was subsequently expanded in several ways. One idea was to greatly increase the number of divisions around the circle to 28, comprised of 14 bipolar pairs of emotions (calm–tension, certainty–uncertainty, compassion–anger, fun–boredom, pleasantness–unpleasantness, happiness–sadness, pleasure–pain, satisfaction–frustration, desire–reject, love–hate, courage–fear, strength–tiredness, enthusiasm–apathy, arrogance–humiliation). Opposing emotions in each pair are situated on opposite sides of the circle, and emotions are ordered around the circle so that similar emotions are adjacent; the earlier concept of two orthogonal axes, pleasantness and arousal, was also retained (Diaz et al. 2001). Another strategy was to add a third dimension. Figure 6 shows an example with somewhat similar ordering of categories around a circle, but with a third dimension depicting intensity (Plutchik 2001).

Figure 6: Three-dimensional circumplex model. The terms in black lettering around the circle represent the primary emotions. There are four pairs of primary dyads, with the contrasting type on the opposite side of the circle. The dyads are arranged so that similar emotions are adjacent, as in a color wheel. Colored regions represent gradations between the primary emotions. Emotional intensity is represented by the radius of concentric circles, folded to create a three-dimensional structure where intensity is the third dimension, as shown in the inset. This model does not reflect the orthogonal pleasantness and arousal axes of the earlier models. (After Plutchik 2001.)

The most recent models have used multivariate statistical analysis of a large number of variables describing different emotions, including appraisal, psychophysiological changes, motor expressions, action tendencies, subjective experiences, and level of emotional regulation and control to statistically sort out the number of dimensions needed to encompass all of the emotional terms. This type of analysis finds that three or four dimensions are required: hedonic valence, arousal, degree of control or power, and unpredictability (Laukka et al. 2005; Fontaine et al. 2007). One such model is illustrated in main text Figure 16.26. Although affective neurobiologists do not find these psychological models helpful, it could turn out to be the case that the emotional axes do correspond to levels of analysis of emotional contexts in the brain. Certainly the amygdala performs an initial analysis of valence (positive or negative), and dopamine and serotonin circuits then determine the motivation or arousal level. Emotions that are close to each other on the wheel may use more overlapping components of the neural circuits, and combination emotions may vary and balance the ratios of different neurotransmitters. As new techniques are developed for monitoring subtle neuronal and chemical changes in the brain in behaving animals, the differences and similarities among emotions may be better elucidated (Panksepp 2003a; Tye et al. 2011).

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