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Review
. 2011;6(9):e21236.
doi: 10.1371/journal.pone.0021236. Epub 2011 Sep 7.

Cross-species affective neuroscience decoding of the primal affective experiences of humans and related animals

Affiliations
Review

Cross-species affective neuroscience decoding of the primal affective experiences of humans and related animals

Jaak Panksepp. PLoS One. 2011.

Abstract

Background: The issue of whether other animals have internally felt experiences has vexed animal behavioral science since its inception. Although most investigators remain agnostic on such contentious issues, there is now abundant experimental evidence indicating that all mammals have negatively and positively-valenced emotional networks concentrated in homologous brain regions that mediate affective experiences when animals are emotionally aroused. That is what the neuroscientific evidence indicates.

Principal findings: The relevant lines of evidence are as follows: 1) It is easy to elicit powerful unconditioned emotional responses using localized electrical stimulation of the brain (ESB); these effects are concentrated in ancient subcortical brain regions. Seven types of emotional arousals have been described; using a special capitalized nomenclature for such primary process emotional systems, they are SEEKING, RAGE, FEAR, LUST, CARE, PANIC/GRIEF and PLAY. 2) These brain circuits are situated in homologous subcortical brain regions in all vertebrates tested. Thus, if one activates FEAR arousal circuits in rats, cats or primates, all exhibit similar fear responses. 3) All primary-process emotional-instinctual urges, even ones as complex as social PLAY, remain intact after radical neo-decortication early in life; thus, the neocortex is not essential for the generation of primary-process emotionality. 4) Using diverse measures, one can demonstrate that animals like and dislike ESB of brain regions that evoke unconditioned instinctual emotional behaviors: Such ESBs can serve as 'rewards' and 'punishments' in diverse approach and escape/avoidance learning tasks. 5) Comparable ESB of human brains yield comparable affective experiences. Thus, robust evidence indicates that raw primary-process (i.e., instinctual, unconditioned) emotional behaviors and feelings emanate from homologous brain functions in all mammals (see Appendix S1), which are regulated by higher brain regions. Such findings suggest nested-hierarchies of BrainMind affective processing, with primal emotional functions being foundational for secondary-process learning and memory mechanisms, which interface with tertiary-process cognitive-thoughtful functions of the BrainMind.

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Conflict of interest statement

Competing Interests: The author has declared that no competing interests exist.

Figures

Figure 1
Figure 1. A truth diagram of anthropomorphism.
A truth diagram relating how we need to think about the possible affective nature of animals (The true nature of the world) and our corresponding scientific judgments about the world. Most of the 20th century was spent believing that the right lower corner was the correct place to be philosophically so one could avoid Type I errors, namely concluding something that is not true to be scientifically correct. This led to discussions of “anxiety-like” behaviors in animals as opposed to fear in animals. This article is premised on the data-based conclusion that individuals who are conversant with the relevant data are wise to situate themselves in the upper left quadrant, since that way we can avoid Type II errors, namely the failure to detect a real phenomenon, because we have false beliefs, or inadequate methods to evaluate the presence of a phenomenon.
Figure 2
Figure 2. Levels of control in brain emotion-affective processing.
A summary of the global levels of control within the brain 1) with 3 general types of affects (red), 2) three types of basic learning mechanisms (green), and 3) three representative awareness functions (blue) of the neocortex (which relies completely on multiple levels of integration, with descending controls down through the basal ganglia to the thalamus, looping back to neocortex) before it can fully elaborate both thoughts and behavior).
Figure 3
Figure 3. Nested hierarchies of control within the brain.
A summary of the hierarchical bottom-up and top-down (circular) causation that is proposed to operate in every primal emotional system of the brain. The schematic summarizes the hypothesis that in order for higher MindBrain functions to mature and function (via bottom-up control), they have to be integrated with the lower BrainMind functions, with primary-processes being depicted as squares (red), secondary-process learning as circles (green), and tertiary processes, by rectangles (blue). The color-coding aims to convey the manner in which nested-hierarchies are integrating lower brain functions into higher brain functions to eventually exert top-down regulatory control (adapted from Northoff, et al. [47]).
Figure 4
Figure 4. Overview of brain arousals and inhibitions.
An overview of brain arousals (reds and yellows) and inhibitions (purples) depicted on lateral surfaces of the right and left hemispheres (top of each panel) and medial surfaces of the corresponding hemispheres (bottom of each panel), while humans experience various basic emotions evoked by autobiographical reminiscing: Upper left: sadness/GRIEF; upper right: happiness/JOY; lower left: anger/RAGE; lower right: anxiety/FEAR (data from Damasio, et al. ; overall patterns of activation and inhibition graciously provided by Antonio Damasio). To highlight the directionality of changes, as monitored by changes in blood flow, inhibitions are indicated by downward arrows (predominating in neocortical regions), while arousals are depicted by upward arrows (predominantly in subcortical regions where emotional behaviors can be evoked by brain stimulation in animals).
Figure 5
Figure 5. Overview of key neuroanatomies and neurochemistries of the primary-process emotional networks.

References

    1. Grandin T. Animals make us human. New York: Houghton Mifflin; 2009.
    1. Panksepp J. Affective neuroscience: The foundations of human and animal emotions. New York: Oxford University Press; 1998.
    1. Panksepp J. Affective consciousness: Core emotional feelings in animals and humans. Consciousness and Cognition. 2005;14:30–80. - PubMed
    1. Mendl M, Burman OHP, Paul ES. An integrative and functional framework for the study of animal emotions and mood. Proceedings of the Royal Society B. 2010;277:2895–2904. - PMC - PubMed
    1. Panksepp J. Affective consciousness in animals: perspectives on dimensional and primary process emotion approaches. Proceedings of the Royal Society B. 2010;277:2905–2907. - PMC - PubMed

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