Jaak Panksepp

Toward a general psychobiological theory of emotions

Emotions seem to arise ultimately from hard-wired neural circuits in the visceral-limbic brain that facilitate diverse and adaptive behavioral and physiological responses to major classes of environmental challenges. Presumably these circuits developed early in mammalian brain evolution, and the underlying control mechanisms remain similar in humans and “lower” mammals. This would suggest that theoretically guided studies of the animal brain can reveal how primitive emotions are organized in the human brain. Conversely, granted this cross-species heritage, it is arguable that human introspective access to emotional states may provide direct information concerning operations of emotive circuits and thus be a primary source of hypotheses for animal brain research. In this article the possibility that emotions are elaborated by transhypothalamic executive (command) circuits that concurrently activate related behavior patterns is assessed. Current neurobehavioral evidence indicates that there are at least four executive circuits of this type – those which elaborate central states of expectancy, rage, fear, and panic. The manner in which learning and psychiatric disorders may arise from activities of such circuits is also discussed.

Brain substrates of infant-mother attachment : Contributions of opioids, oxytocin, and norepinephrine

The aim of this paper is to review recent work concerning the psychobiological substrates of social bonding, focusing on the literature attributed to opioids, oxytocin and norepinephrine in rats. Existing evidence and thinking about the biological foundations of attachment in young mammalian species and the neurobiology of several other affiliative behaviors including maternal behavior, sexual behavior and social memory is reviewed. We postulate the existence of social motivation circuitry which is common to all mammals and consistent across development. Oxytocin, vasopressin, endogenous opioids and catecholamines appear to participate in a wide variety of affiliative behaviors and are likely to be important components in this circuitry. It is proposed that these same neurochemical and neuroanatomical patterns will emerge as key substrates in the neurobiology of infant attachments to their caregivers.

Neurobiology of 50-kHz ultrasonic vocalizations in rats: Electrode mapping, lesion, and pharmacology studies

Fifty-kHz ultrasonic vocalizations have been proposed to reflect a positive appetitive affective state in rats, being consistently linked to the positive appetitive behavior. In the first study, we examined the brain substrates of 50-kHz ultrasonic vocalizations (USVs) by using localized electrical stimulation of the brain (ESB) at various sites that are known to mediate reward. We found that the brain areas that produced ESB-induced 50-kHz calls are the areas that have previously been shown to support the most vigorous self-stimulation behavior (prefrontal cortex, nucleus accumbens, ventral pallidum, lateral preoptic area, lateral hypothalamus, ventral tegmental area, and raphe). Importantly, all animals that showed repeatable ESB-induced 50-kHz USVs demonstrated self-stimulation behavior. In the second study, conditioned place preference was assessed following microinjection of the mu-opiate agonist Tyr-D-Ala-Gly-N-methyl-Phe-Gly-ol (DAMGO) directly into the ventral tegmental area (VTA) at a dose previously found to be rewarding. Animals that showed more 50-kHz USVs in response to drug injections compared to vehicle injections showed significant place preferences, whereas animals that did not show elevated vocalization to DAMGO did not show place preference. In experiment 3, we examined the effect of VTA electrolytic lesions, 6-OHDA lesions, and the effect of the D1/D2 dopamine antagonist flupenthixol (0 and 0.8 mg/kg, i.p.) on 50-kHz ultrasonic vocalizations. We found that these manipulations all selectively reduced 50-kHz ultrasonic vocalizations, and that these effects could be disassociated from any side effects. These data are consistent with the proposition that 50-kHz calls are tightly linked to reward in rats and that the neural circuit of 50-kHz calls closely overlaps that of ESB self-stimulation reward, drug reward, and the mesolimbic dopamine system.

Endogenous opioids and social behavior

Evidence for the hypothesis that brain-opioids mediate social affect and social attachments is summarized. Opiates and opioids are very effective in reducing social separation-induced distress vocalizations (DVs), in puppies, young guinea pigs and chicks, while opiate antagonists can increase DVs. In studies of specific social behaviors in rodents, morphine (at doses 1 mg/kg and below) decreases proximity maintenance time in socially housed animals, increased play, decreases maternal aggression but has no effect on pup retrieval. Naloxone reduces play and disrupts pup-retrieval, but has no consistent effect on proximity maintenance time of socially housed animals. In young rats tested in social learning situations, morphine delays and naloxone hasten extinction. These data are consistent with the proposition that brain opioids modulate social emotions and behaviors.

Nucleus accumbens amphetamine microinjections unconditionally elicit 50-kHz ultrasonic vocalizations in rats.

The authors have hypothesized that, in adult rats, 50-kHz ultrasonic vocalizations (USVs) index a state characterized by high arousal and expectations of reward. This study was conducted to investigate whether dopamine agonism of the nucleus accumbens (NAcc) could evoke such an appetitive state, by examining the effects of NAcc amphetamine (AMPH) microinjections on USVs. Intra-NAcc AMPH injections (0.3, 1.0, 3.0, 10.0 microg unilaterally) produced robust, dose-dependent increases in 50-kHz USVs, which could not be accounted for by concomitant increases in locomotor activity (LA). However, AMPH injections into dorsal control caudate putamen sites produced a modest, dose-dependent increase in LA without significant increases in 50-kHz USVs. These findings indicate that NAcc AMPH microinjections selectively evoke 50-kHz USVs in rats, supporting the notion that dopamine elevations in the NAcc may unconditionally elicit a state of reward anticipation.

The neurobiology of positive emotions

Compared to the study of negative emotions such as fear, the neurobiology of positive emotional processes and the associated positive affect (PA) states has only recently received scientific attention. Biological theories conceptualize PA as being related to (i) signals indicating that bodies are returning to equilibrium among those studying homeostasis, (ii) utility estimation among those favoring neuroeconomic views, and (iii) approach and other instinctual behaviors among those cultivating neuroethological perspectives. Indeed, there are probably several distinct forms of positive affect, but all are closely related to ancient sub-neocortical limbic brain regions we share with other mammals. There is now a convergence of evidence to suggest that various regions of the limbic system, including especially ventral striatal dopamine systems are implemented in an anticipatory (appetitive) positive affective state. Dopamine independent mechanisms utilizing opiate and GABA receptors in the ventral striatum, amygdala and orbital frontal cortex are important in elaborating consummatory PA (i.e. sensory pleasure) states, and various neuropeptides mediate homeostatic satisfactions.

Sleep as a fundamental property of neuronal assemblies

Sleep is vital to cognitive performance, productivity, health and well-being. Earlier theories of sleep presumed that it occurred at the level of the whole organism and that it was governed by central control mechanisms. However, evidence now indicates that sleep might be regulated at a more local level in the brain: it seems to be a fundamental property of neuronal networks and is dependent on prior activity in each network. Such local-network sleep might be initiated by metabolically driven changes in the production of sleep-regulatory substances. We discuss a mathematical model which illustrates that the sleep-like states of individual cortical columns can be synchronized through humoral and electrical connections, and that whole-organism sleep occurs as an emergent property of local-network interactions.

The psychobiology of play: Theoretical and methodological perspectives ☆

The social play of pairs of juvenile rats can be brought under tight experimental control using social deprivation, and it can be objectively quantified by measurement of pinning behavior. Research and conceptual issues concerning this paired-encounter procedure are summarized, including issues related to measurement, gender differences (and the absence thereof), relations between play and aggression, the regulatory processes interacting with and underlying play, the neurochemical and neuroanatomical substrates of play, the functions of play in dominance and other adult behaviors. Existing results suggest the operation of a harmoniously operating brain process which generates a unique emotive brain process that is appropriately referred to as social play. Although the concept of play remains to be adequately defined, the position is advocated that rigorous psychobiological analysis will ultimately provide an empirical definition based upon neural circuit characteristics. Analysis of the underlying circuits may help reveal the manner in which more complex levels of behavioral competence arise ontogenically, and work in the area may yield clues to the genesis of several psychopathologies.

ANTICIPATION OF PLAY ELICITS HIGH-FREQUENCY ULTRASONIC VOCALIZATIONS IN YOUNG RATS

The authors provide initial documentation that juvenile rats emit short, high-frequency ultrasonic vocalizations (high USVs, approximately 55 kHz) during rough-and-tumble play. In an observational study, they further observe that these vocalizations both correlate with and predict appetitive components of the play behavioral repertoire. Additional experiments characterized eliciting conditions for high USVs. Without prior play exposure, rats separated by a screen vocalized less than playing rats, but after only 1 play session, separated rats vocalized more than playing rats. This findings suggested that high USVs were linked to a motivational state rather than specific play behaviors or general activity. Furthermore, individual rats vocalized more in a chamber associated with play than in a habituated control chamber. Finally, congruent and incongruent motivational manipulations modulated vocalization expression. Although play deprivation enhanced high USVs, an arousing but aversive stimulus (bright light) reduced them. Taken together, these findings suggest that high USVs may index an appetitive motivation to play in juvenile rats.

Social deprivation and play in rats

Social interaction (play fighting) was studied in socially housed and individually housed juvenile rats (18–30 days of age). Pinning (an animal on its back, with the other on top) proved to be a simple measure of play which correlated highly with other measures of playful behavior (solicitive behaviors, following, rough-and-tumble play, and together-time measures). Play behaviors were markedly increased by social deprivation and reduced by social satiation. The results suggest that social play is a regulated process which can be easily quantified by the simple and objective measure of pinning behavior.