What is an emotional feeling? Lessons about affective origins from cross-species neuroscience

Cross-species affective neuroscience aspires to provide an evidence-based foundation for understanding the primary-process emotional networks that concurrently control instinctual emotional actions and affective feelings—direct emotional circuit mediated ‘rewards’ and ‘punishments’. In humans and other mammals, the ancestral subcortical regions of the brain are central to such affective BrainMind functions (a monistic term, here used synonymously with MindBrain, depending on stylistic needs). Although these circuits cannot be ‘identical’ across species (that would be incompatible with evolutionary principles) they are sufficiently similar, anatomically, neurochemically and functionally, to allow animal brain research to illuminate (yield testable predictions) about homologous human mind functions. Primal emotional feelings (affects) are inbuilt value functions of the brain that energize and inform the rest of the mental apparatus about basic survival values, thereby promoting secondary-process learning/memory functions and tertiary-process cognitive thinking-ruminative functions, yielding bottom-up evolutionary controls that ultimately allow top-down regulatory controls. As we envision how such “nested” hierarchies—two-way paths of causality—reflecting both bottom-up and top-down functions—we will need disciplined distinctions between cognitions and emotions at the primary-process level, while also accepting total interpenetrance of cognitions and affects at the tertiary-process level of MindBrain organization. This allows full and synergistic integration of basic and dimensional approaches to emotions. Here the primal emotional networks, so critically important for understanding ‘human-nature’ and psychiatric disorders, are discussed didactically in ways that can minimize dilemmas that non-evolutionary, non-hierarchical perspectives are subject to in modern emotion research.

[1]  Jaak Panksepp,et al.  Neuroevolutionary sources of laughter and social joy: Modeling primal human laughter in laboratory rats , 2007, Behavioural Brain Research.

[2]  H. Pashler,et al.  Puzzlingly High Correlations in fMRI Studies of Emotion, Personality, and Social Cognition 1 , 2009, Perspectives on psychological science : a journal of the Association for Psychological Science.

[3]  E. Costello,et al.  Child μ-Opioid Receptor Gene Variant Influences Parent–Child Relations , 2011, Neuropsychopharmacology.

[4]  Nakia S. Gordon,et al.  Modeling ADHD-type arousal with unilateral frontal cortex damage in rats and beneficial effects of play therapy , 2003, Brain and Cognition.

[5]  E. Nestler,et al.  Linking molecules to mood: new insight into the biology of depression. , 2010, The American journal of psychiatry.

[6]  I. McGilchrist,et al.  The Master and His Emissary: The Divided Brain and the Making of the Western World , 2009 .

[7]  Joseph E LeDoux The emotional brain , 1996 .

[8]  Volker A Coenen,et al.  Tractographic Analysis of Historical Lesion Surgery for Depression , 2010, Neuropsychopharmacology.

[9]  J. Panksepp,et al.  Effects of beta-chlornaltrexamine on separation distress in chicks. , 1982, Life sciences.

[10]  M. Raichle The Brain's Dark Energy , 2006, Science.

[11]  M. Mendl,et al.  An integrative and functional framework for the study of animal emotion and mood , 2010, Proceedings of the Royal Society B: Biological Sciences.

[12]  J. Panksepp,et al.  Why Does Depression Hurt? Ancestral Primary-Process Separation-Distress (PANIC/GRIEF) and Diminished Brain Reward (SEEKING) Processes in the Genesis of Depressive Affect , 2011, Psychiatry.

[13]  J. Panksepp Textbook of Biological Psychiatry , 2003 .

[14]  Michael X. Cohen,et al.  Nucleus Accumbens Deep Brain Stimulation Decreases Ratings of Depression and Anxiety in Treatment-Resistant Depression , 2010, Biological Psychiatry.

[15]  D. Schutter,et al.  An endocrine perspective on the role of steroid hormones in the antidepressant treatment efficacy of transcranial magnetic stimulation , 2010, Psychoneuroendocrinology.

[16]  R. M. Stutz,et al.  Discriminability of intracranial stimuli: the role of anatomical connectedness. , 1974, Physiology & behavior.

[17]  Bezerra Ml,et al.  Transient acute depression induced by high-frequency deep-brain stimulation. , 1999 .

[18]  Hans-Jochen Heinze,et al.  Differential parametric modulation of self‐relatedness and emotions in different brain regions , 2009, Human brain mapping.

[19]  D. Goleman Social Intelligence: The New Science of Human Relationships , 2006 .

[20]  R. Koeppe,et al.  Regulation of human affective responses by anterior cingulate and limbic mu-opioid neurotransmission. , 2003, Archives of general psychiatry.

[21]  J. Panksepp,et al.  Cross-species affective functions of the medial forebrain bundle—Implications for the treatment of affective pain and depression in humans , 2011, Neuroscience & Biobehavioral Reviews.

[22]  J. Panksepp Affective Neuroscience: The Foundations of Human and Animal Emotions , 1998 .

[23]  J. Panksepp On the Embodied Neural Nature of Core Emotional Affects , 2005 .

[24]  W. James,et al.  What Is an Emotion , 1977 .

[25]  Robert C. Solomon,et al.  What is an emotion? : classic and contemporary readings , 2003 .

[26]  Robin I. M. Dunbar,et al.  Oxford handbook of evolutionary psychology , 2007 .

[27]  K. Deisseroth,et al.  Circuit-breakers: optical technologies for probing neural signals and systems , 2007, Nature Reviews Neuroscience.

[28]  J. Panksepp Affective consciousness: Core emotional feelings in animals and humans , 2005, Consciousness and Cognition.

[29]  B. Skinner,et al.  Science and human behavior , 1953 .

[30]  A. Jersild,et al.  Feelings and Emotions. , 1929 .

[31]  Georg Northoff,et al.  Is subcortical–cortical midline activity in depression mediated by glutamate and GABA? A cross-species translational approach , 2010, Neuroscience & Biobehavioral Reviews.

[32]  Katherine Vytal,et al.  Neuroimaging Support for Discrete Neural Correlates of Basic Emotions: A Voxel-based Meta-analysis , 2010, Journal of Cognitive Neuroscience.

[33]  J. Panksepp,et al.  Mental health and well-being in animals , 2005 .

[34]  Michael X. Cohen,et al.  Deep Brain Stimulation to Reward Circuitry Alleviates Anhedonia in Refractory Major Depression , 2008, Neuropsychopharmacology.

[35]  J. Panksepp,et al.  The role of emotional systems in addiction: a neuroethological perspective. , 2004, Nebraska Symposium on Motivation. Nebraska Symposium on Motivation.

[36]  A. Ortony,et al.  What's basic about basic emotions? , 1990, Psychological review.

[37]  Agneta H. Fischer,et al.  Feelings and Emotions: The Amsterdam Symposium , 2004 .

[38]  Y Agid,et al.  Transient acute depression induced by high-frequency deep-brain stimulation. , 1999, The New England journal of medicine.

[39]  P. Griffiths What emotions really are : the problem of psychological categories , 1997 .

[40]  W P Wilson,et al.  Sensations evoked by stimulation in the midbrain of man. , 1969, Journal of neurosurgery.

[41]  J. Russell Core affect and the psychological construction of emotion. , 2003, Psychological review.

[42]  Brian Knutson,et al.  The role of brain emotional systems in addictions: a neuro-evolutionary perspective and new 'self-report' animal model. , 2002, Addiction.

[43]  Jaak Panksepp,et al.  Primary Process Affects and Brain Oxytocin , 2009, Biological Psychiatry.

[44]  J. Panksepp,et al.  Opioid blockade and social comfort in chicks , 1980, Pharmacology Biochemistry and Behavior.

[45]  W. James II.—WHAT IS AN EMOTION ? , 1884 .

[46]  D. Denton The Primordial Emotions: The Dawning of Consciousness , 2006 .

[47]  J. Panksepp Toward a cross‐species neuroscientific understanding of the affective mind: do animals have emotional feelings? , 2011, American journal of primatology.

[48]  J. Panksepp,et al.  Imaging Human Emotions and Affective Feelings: Implications for Biological Psychiatry , 2004 .

[49]  Kent C. Berridge,et al.  Feelings and Emotions: Pleasure, Unfelt Affect, and Irrational Desire , 2004 .

[50]  Satoshi Ikemoto,et al.  Brain reward circuitry beyond the mesolimbic dopamine system: A neurobiological theory , 2010, Neuroscience & Biobehavioral Reviews.

[51]  J Leon Kenemans,et al.  How Human Electrophysiology Informs Psychopharmacology: from Bottom-up Driven Processing to Top-Down Control , 2011, Neuropsychopharmacology.

[52]  Richard J. Davidson,et al.  Seven sins in the study of emotion: Correctives from affective neuroscience , 2003, Brain and Cognition.

[53]  L. F. Barrett Are Emotions Natural Kinds? , 2006, Perspectives on psychological science : a journal of the Association for Psychological Science.

[54]  William Rowan,et al.  The Study of Instinct , 1953 .

[55]  Benjamin D. Greenberg,et al.  What's in a “Smile?” Intra-operative Observations of Contralateral Smiles Induced by Deep Brain Stimulation , 2004, Neurocase.

[56]  Volker A Coenen,et al.  MEDIAL FOREBRAIN BUNDLE STIMULATION AS A PATHOPHYSIOLOGICAL MECHANISM FOR HYPOMANIA IN SUBTHALAMIC NUCLEUS DEEP BRAIN STIMULATION FOR PARKINSON'S DISEASE , 2009, Neurosurgery.

[57]  J. Hirsch,et al.  Neural Mechanisms of Grief Regulation , 2009, Biological Psychiatry.

[58]  Samet Kose,et al.  Brain basis of early parent-infant interactions: psychology, physiology, and in vivo functional neuroimaging studies. , 2007, Journal of child psychology and psychiatry, and allied disciplines.

[59]  N. Tinbergen,et al.  The Study of Instinct , 1953 .

[60]  R. Depue,et al.  Neurobiology of the structure of personality: Dopamine, facilitation of incentive motivation, and extraversion , 1999, Behavioral and Brain Sciences.

[61]  Axel Cleeremans,et al.  The Oxford Companion to Consciousness , 2009 .

[62]  Jaak Panksepp,et al.  Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: Behavioral concomitants, relationship to reward, and self-administration of playback. , 2008, Journal of comparative psychology.

[63]  Phoebe C. Ellsworth William James and Emotion: Is a Century of Fame Worth a Century of Misunderstanding? , 1994 .

[64]  S. Hyman,et al.  Animal models of neuropsychiatric disorders , 2010, Nature Neuroscience.

[65]  J. Panksepp At the interface of the affective, behavioral, and cognitive neurosciences: Decoding the emotional feelings of the brain , 2003, Brain and Cognition.

[66]  Jaak Panksepp,et al.  Toward a general psychobiological theory of emotions , 1982, Behavioral and Brain Sciences.

[67]  J. Panksepp,et al.  Positive affective vocalizations during cocaine and sucrose self-administration: A model for spontaneous drug desire in rats , 2011, Neuropharmacology.

[68]  C. Darwin,et al.  The Expression of the Emotions in Man and Animals , 1872 .

[69]  J. Panksepp,et al.  The Archaeology of Mind: Neuroevolutionary Origins of Human Emotions , 2012 .

[70]  P. Pollak,et al.  Transient acute depression induced by high-frequency deep-brain stimulation. , 1999, The New England journal of medicine.

[71]  J. Panksepp,et al.  The ‘resting-state hypothesis’ of major depressive disorder—A translational subcortical–cortical framework for a system disorder , 2011, Neuroscience & Biobehavioral Reviews.

[72]  A. Damasio,et al.  Subcortical and cortical brain activity during the feeling of self-generated emotions , 2000, Nature Neuroscience.

[73]  J. Panksepp,et al.  Neurobiology of 50-kHz ultrasonic vocalizations in rats: Electrode mapping, lesion, and pharmacology studies , 2007, Behavioural Brain Research.