''Laughing'' Rats and the Evolutionary Antecedents of Human Joy?

Physiology & Behavior 79 (2003) 533–547 ‘‘Laughing’’ rats and the evolutionary antecedents of human joy? Jaak Pankseppa,b,*, Jeff Burgdorf a aDepartment of Psychology, J.P. Scott Center for Neuroscience, Mind and Behavior, Bowling Green State University, Bowling Green, OH 43403, USA bFalk Center for Molecular Therapeutics, Northwestern University Research Park, 1801 Maple Avenue, Suite 4306, Evanston, IL 60201, USA Received 4 April 2003; accepted 17 April 2003 Abstract Paul MacLean’s concept of epistemics—the neuroscientific study of subjective experience—requires animal brain research that can be related to predictions concerning the internal experiences of humans. Especially robust relationships come from studies of the emotional/ affective processes that arise from subcortical brain systems shared by all mammals. Recent affective neuroscience research has yielded the discovery of play- and tickle-induced ultrasonic vocalization patterns ( 50-kHz chirps) in rats may have more than a passing resemblance to primitive human laughter. In this paper, we summarize a dozen reasons for the working hypothesis that such rat vocalizations reflect a type of positive affect that may have evolutionary relations to the joyfulness of human childhood laughter commonly accompanying social play. The neurobiological nature of human laughter is discussed, and the relevance of such ludic processes for understanding clinical disorders such as attention deficit hyperactivity disorders (ADHD), addictive urges and mood imbalances are discussed. D 2003 Published by Elsevier Inc. Keywords: Laughter; Ultrasonic vocalizations; Joy; Attention deficit hyperactivity disorders; Addictions; Mood disorders; Rats 1. Introduction lenge the existence of a variety of evolved emotional systems that we still share with other mammals. One of Paul MacLean’s lasting insights was the recog- That creatures as lowly as crayfish and planaria exhibit nition that subcortical regions of the mammalian brain place preferences for drugs that human desire [42,71] also contain a variety of evolved emotional systems for the coaxes us to consider the utility of subtle concepts such as governance of behavior. He accepted the likelihood that affect-psychological processes that are created by ancient subjective emotional experiences arise from specifiable value-encoding, neural systems of the brain. To our way of neural systems, and he encapsulated his interest in the thinking, affects are the currency of the brain/mind economy fundamental nature of such psychobiological functions in that signal the survival value of objects and ways of acting the concept of epistemics—the study of ‘‘the subjective self in the world. Thus, there are natural categories of affective and its relations to the internal and external environment’’ processes—some linked to sensing the fruits and dangers of [48, p. 6]. Furthermore, he suggested that the brain regions the world, some related to anticipation of positive and which govern basic emotional urges exhibit an impressive negative events, some related to actions in the world, and functional and anatomical coherence that deserves special some related to postconsummatory reactions. All may re- recognition. Thereby, his concept of the limbic system quire some type of primitive neural structure that can be emerged as one of the great memes of functional neurosci- conceptualized as the ‘‘core self’’ [20,55,57]. Our working ence. Recently, an increasing number of neurobehaviorists premise is that affects are intrinsic aspects of emotional have challenged the utility of this concept (e.g., Ref. [45]) operating systems in the brain, and thereby constitute albeit no neuroscientist has had adequate reason to chal- centers of gravity around which the decision making and operational/instrumental features of the surrounding cognitive processes revolve. In the present paper, we will focus on * Corresponding author. Department of Psychology, J.P. Scott Center our recent discovery of a vocal pattern in rats which may for Neuroscience, Mind and Behavior, Bowling Green State University, Bowling Green, OH 43403, USA. Tel.: +1-419-372-2819; fax: +1-419-372- have evolutionary relationships to laughter, and hence, fun- 6013. damentally to joyful social processes that are carried out by E-mail address: [email protected] (J. Panksepp). the mammalian brain. 0031-9384/$ – see front matter D 2003 Published by Elsevier Inc. doi: 10.1016/S0031-9384(03)00159-8 534 J. Panksepp, J. Burgdorf / Physiology & Behavior 79 (2003) 533–547 2. The brain systems for affective experience not match up, and many of the neurochemistries that are of interest (e.g., catecholamines) can have direct effects on During the past three decades, enormous progress has blood flow dynamics that may be independent of neural been made in characterizing the brain systems that promote dynamics. Still, when we look at the best brain imaging that reproduction (sexual and maternal nurturance systems) and has been done of human emotional experience [21], there is related social processes that help newborn animals to signal a striking correspondence to what we know about the social distress and social excitement (i.e., separation distress localization of emotional circuits in the brains of other and playfulness) both of which promote social bonding, the mammals [55,59,60]. development of social skills, and thereby the competence to Despite massive evidence suggesting conservation of sustain generative cycle of life [55,70]. Such evolved neu- principles across all mammalian species among the subcor- robehavioral tools, honed exquisitely and at times idiosyn- tical systems that govern basic emotions and motivations, cratically by individual learning experiences, help establish the detailed study of neural circuits that control animal communicative urges that support our human neurosymbolic emotions remains to be generally accepted as being of capacities for refined forms of intersubjectivity (reflected fundamental importance for understanding human emotions. most clearly in our abiding interest in the contents of other Partly, this simply reflects the fact that deep evolutionary minds) [87]. Among the basic social signaling systems, considerations do not yet guide thinking in the field [68], audiovocal and presemantic forms of social communication and partly, the natural tendency of scholars to resist assim- [48] may be the antecedents to the social urges that charac- ilation of the types of findings in which they have not been terize human life. However, the linkages between what we active participants. Thus, we are left with the dilemma that know about the human mind and what we know about some basic neuroscientists agonize over the extent to which animal brain functions remain a difficult and contentious their empirical victories in studying the brains of animals topic, and the needed empirical bridges remain to be con- relevant for the understanding our own species. The evolu- structed with disciplinary conviction. tionary perspective provides a clear answer—at a subcorti- Those who do not work on these brain systems typically cal level, where anatomical and neurochemical homologies remain skeptical of the relevance of this knowledge for abound, there are bound to be remarkable functional simi- understanding the human condition, even though a careful larities [68], unless, of course, these lower functions have analysis of the data collected during the era of psychosur- become vestigial for human behavior. Although there has gery provided some impressive data concerning the simi- continued to be considerable evolutionary divergence in the larity of human and animal subcortical emotional functions details of emotional brain mechanisms across species, there [33]. Still, even with modern brain imaging, the details of is presently no empirical reason to believe such fundamental the neural circuits that govern human emotions and moti- brain operating systems have become vestigial in any vations remain largely outside the realm of neuroscientific mammalian species, even though it is likely they can be inquiry. The existing imaging techniques only identify decisively inhibited and regulated by the emergence of regions of interest for further analyses. When it comes to various higher brain functions, most dramatically the im- the cardinal issue of identifying causal processes for mam- pressive cognitive capacities of humans. malian emotional feelings, these techniques are susceptible Paul MacLean was one of the few who had the intellectual to abundant false negatives as well as an indeterminate courage to deal directly with the implications of ancient number of false positives since they highlight correlated limbic brain systems for understanding human emotions. rather than causal aspects of core emotions. Indeed, such Ultimately such neuroevolutionary perspectives must be technologies are not especially robust for visualizing brain- evaluated by the new predictions they can generate, especial- stem functions. For instance, the widespread use of sensory ly for the human species. For instance, the neurochemical stimuli to evoke emotions typically leaves open the question issues have become especially tractable—there are examples of how much the resulting brain arousals reflect nonaffec- of how effectively our understanding of biogenic amine tive perceptual processes as opposed to brain functions that systems in animal models has guided an understanding of actively generate affective experience. Indeed, there is

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