The role of brain emotional systems in addictions: a neuro-evolutionary perspective and new 'self-report' animal model.

The evolutionary significance of neurochemical events in the brain has received minimal attention in the field of addiction research. Likewise, the general failure of neuroscientists to postulate how basic brain circuits might mediate emotional urges has retarded the development of scientific perspectives that could inform new inquiries into the underlying dynamics and treatment of addictions. In this paper, we revisit the argument that prototypically abused substances activate or alter specific emotional brain systems that were evolutionarily designed to signal potential increments or decrements in fitness. We then discuss two distinct emotional systems (reward seeking and separation distress) which may track different types of potential changes in fitness. Based on this evolutionarily inspired approach, we illustrate how a mammalian model of emotion (i.e. rodent ultrasonic vocalizations) may enable scientists to predict drug-related phenomena such as abuse potential, anatomical location of mediating neural substrates, and the psychological impact of withdrawal. We conclude by discussing some therapeutic and social implications of examining drug addiction processes with multiple emotional brain systems in mind.

[1]  M. Blumberg,et al.  On the significance of similarities between ultrasonic vocalizations of infant and adult rats , 1991, Neuroscience & Biobehavioral Reviews.

[2]  J. Whelan,et al.  Cocaine : scientific and social dimensions , 1992 .

[3]  R. Foltin,et al.  Self-administration of cocaine by humans: a laboratory perspective. , 1992, Ciba Foundation symposium.

[4]  A. Tellegen,et al.  Genetic and Environmental Influences on Religious Interests, Attitudes, and Values: A Study of Twins Reared Apart and Together , 1990 .

[5]  Appetites and Aversions as Constituents of Instincts. , 1918, Proceedings of the National Academy of Sciences of the United States of America.

[6]  S. Ikemoto,et al.  The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking , 1999, Brain Research Reviews.

[7]  N. Rathod Society for the Study of Addiction , 1977 .

[8]  M. Linnoila,et al.  Nonhuman primate model of alcohol abuse: effects of early experience, personality, and stress on alcohol consumption. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[9]  K. Berridge,et al.  The neural basis of drug craving: An incentive-sensitization theory of addiction , 1993, Brain Research Reviews.

[10]  N. S. Miller,et al.  Integration of generalized vulnerability to drug and alcohol addiction. , 1997, Journal of addictive diseases.

[11]  J. Panksepp,et al.  Chronic intermittent amphetamine pretreatment enhances future appetitive behavior for drug- and natural-reward: interaction with environmental variables , 2002, Behavioural Brain Research.

[12]  J. Rapoport,et al.  Quantitative brain magnetic resonance imaging in attention-deficit hyperactivity disorder. , 1996, Archives of general psychiatry.

[13]  R. J. Barfield,et al.  Ultrasonic Vocalizations in Rat Sexual Behavior , 1979 .

[14]  K. Scherer Vocal affect expression: a review and a model for future research. , 1986, Psychological bulletin.

[15]  P. Young The role of affective processes in learning and motivation. , 1959, Psychological review.

[16]  S. Paradiso,et al.  Book Review: Affective Neuroscience: The Foundations of Human and Animal Emotions , 2000 .

[17]  J. M. Nelsen,et al.  Clinical and psychological effects of marihuana in man. , 1968, Science.

[18]  K. Berridge,et al.  Psychoactive drug use in evolutionary perspective. , 1997, Science.

[19]  R. Bandler,et al.  Longitudinal neuronal organization of defensive reactions in the midbrain periaqueductal gray region of the rat , 2004, Experimental Brain Research.

[20]  A. Shulgin,et al.  PIHKAL: A Chemical Love Story , 1991 .

[21]  J. Panksepp,et al.  Neural and Neurochemical Control of the Separation Distress Call , 1988 .

[22]  J. Panksepp,et al.  Opiates and play dominance in juvenile rats. , 1985, Behavioral neuroscience.

[23]  L. Brauer,et al.  Subjective responses to d-amphetamine alone and after pimozide pretreatment in normal, healthy volunteers , 1996, Biological Psychiatry.

[24]  C. Marsden,et al.  Effect of social isolation on the reinforcing properties of morphine in the conditioned place preference test , 1996, Pharmacology Biochemistry and Behavior.

[25]  R. Wise,et al.  Dopamine Fluctuations in the Nucleus Accumbens during Maintenance, Extinction, and Reinstatement of Intravenous d-Amphetamine Self-Administration , 1999, The Journal of Neuroscience.

[26]  Cocaine: Scientific and Social Dimensions , 1993 .

[27]  A. Argiolas,et al.  Neuropeptides and sexual behaviour , 1999, Neuroscience & Biobehavioral Reviews.

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

[29]  G. Kovacs,et al.  Role of oxytocin in the neuroadaptation to drugs of abuse , 1994, Psychoneuroendocrinology.

[30]  A. Kelley Functional Specificity of Ventral Striatal Compartments in Appetitive Behaviors , 1999, Annals of the New York Academy of Sciences.

[31]  M. Kimura,et al.  The phosphorylated analogue of DSIP enhances slow wave sleep and paradoxical sleep in unrestrained rats , 2004, Psychopharmacology.

[32]  J. Brobeck The Integrative Action of the Nervous System , 1948, The Yale Journal of Biology and Medicine.

[33]  Brian Knutson,et al.  High-Frequency Ultrasonic Vocalizations Index Conditioned Pharmacological Reward in Rats , 1999, Physiology & Behavior.

[34]  Brian Knutson,et al.  Nucleus accumbens amphetamine microinjections unconditionally elicit 50-kHz ultrasonic vocalizations in rats. , 2001, Behavioral neuroscience.

[35]  J. Panksepp,et al.  Endogenous opioids and social behavior , 1980, Neuroscience & Biobehavioral Reviews.

[36]  C. Patrick,et al.  Alcohol and human emotion: a multidimensional analysis incorporating startle-probe methodology. , 1995, Journal of abnormal psychology.

[37]  H. W. Harris,et al.  Chronic morphine induces visible changes in the morphology of mesolimbic dopamine neurons. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Eric B. Keverne,et al.  Beta-endorphin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships , 1989, Psychoneuroendocrinology.

[39]  Brian Knutson,et al.  Toward a Neuroscience of Emotion , 1998 .

[40]  A. Dodge,et al.  Psychomotor stimulants, social deprivation and play in juvenile rats , 1982, Pharmacology Biochemistry and Behavior.

[41]  P. Ekman Facial expression and emotion. , 1993, The American psychologist.

[42]  P. Kalivas,et al.  Interactions between dopamine and excitatory amino acids in behavioral sensitization to psychostimulants. , 1995, Drug and alcohol dependence.

[43]  J. Westermeyer The role of cultural and social factors in the cause of addictive disorders. , 1999, The Psychiatric clinics of North America.

[44]  Brian Knutson,et al.  Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats. , 1998, Journal of comparative psychology.

[45]  K. Berridge Food reward: Brain substrates of wanting and liking , 1996, Neuroscience & Biobehavioral Reviews.

[46]  M. Kreek Cocaine, dopamine and the endogenous opioid system. , 1996, Journal of addictive diseases.

[47]  D. A. Thomas,et al.  Analysis of ultrasonic vocalizations emitted by intruders during aggressive encounters among rats (Rattus norvegicus). , 1983, Journal of comparative psychology.

[48]  K. Miczek,et al.  Dissociation of consummatory and vocal components of feeding in squirrel monkeys treated with benzodiazepines and alcohol , 1998, Psychopharmacology.

[49]  D. Calsyn,et al.  Interpersonal style differences among drug abusers. , 1988, Journal of clinical psychology.

[50]  K. Berridge,et al.  What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? , 1998, Brain Research Reviews.

[51]  D. Watson,et al.  Toward a consensual structure of mood. , 1985, Psychological bulletin.

[52]  Jaak Panksepp,et al.  Neurochemical control of moods and emotions: Amino acids to neuropeptides. , 1993 .

[53]  Jaak Panksepp,et al.  The seven sins of evolutionary psychology , 2001 .

[54]  Y. Hayashi,et al.  The midbrain central gray substance as a highly sensitive neural structure for the production of ultrasonic vocalization in the rat , 1980, Brain Research.

[55]  J. Panksepp,et al.  The biology of social attachments: opiates alleviate separation distress. , 1978, Biological psychiatry.

[56]  R. Wise Drug-activation of brain reward pathways. , 1998, Drug and alcohol dependence.

[57]  G. Sales,et al.  Ultrasonic Communication by Animals , 1974 .

[58]  K. Preston,et al.  The reinforcing and subjective effects of morphine in post-addicts: a dose-response study. , 1991, The Journal of pharmacology and experimental therapeutics.

[59]  D. C. Blanchard,et al.  Twenty-two kHz alarm cries to presentation of a predator, by laboratory rats living in visible burrow systems , 1991, Physiology & Behavior.

[60]  R. Wise,et al.  Elevations of nucleus accumbens dopamine and DOPAC levels during intravenous heroin self‐administration , 1995, Synapse.

[61]  R. Wise,et al.  Brain dopamine and reward. , 1989, Annual review of psychology.

[62]  C. Patrick,et al.  Beyond stress and arousal: a reconceptualization of alcohol-emotion relations with reference to psychophysiological methods. , 1996, Psychological bulletin.

[63]  M. Gold,et al.  Opiate addiction and the locus coeruleus. The clinical utility of clonidine, naltrexone, methadone, and buprenorphine. , 1993, The Psychiatric clinics of North America.

[64]  W. Hodos,et al.  Comparative Vertebrate Neuroanatomy: Evolution and Adaptation , 2005 .

[65]  S. Brudzyński,et al.  The related roles of dopamine and glutamate in the initiation of 50-kHz ultrasonic calls in adult rats , 2001, Pharmacology Biochemistry and Behavior.

[66]  G F Koob,et al.  Drug dependence: stress and dysregulation of brain reward pathways. , 1998, Drug and alcohol dependence.

[67]  H F HARLOW,et al.  Social deprivation in monkeys. , 1962, Scientific American.

[68]  Joseph E LeDoux Emotion Circuits in the Brain , 2000 .

[69]  James L Olds Drives and reinforcements : behavioral studies of hypothalamic functions / by James Olds , 1977 .

[70]  J. Panksepp,et al.  50-kHz chirping (laughter?) in response to conditioned and unconditioned tickle-induced reward in rats: effects of social housing and genetic variables , 2000, Behavioural Brain Research.

[71]  M McGue,et al.  Behavioral disinhibition and the development of substance-use disorders: Findings from the Minnesota Twin Family Study , 1999, Development and Psychopathology.

[72]  J. Panksepp,et al.  The pharmacology of endorphin modulation of chick distress vocalization , 1984, Peptides.

[73]  M. Meaney,et al.  Maternal care and the development of stress responses , 1999, Current Opinion in Neurobiology.

[74]  J. Panksepp,et al.  The role of brain norepinephrine in clonidine suppression of isolation-induced distress in the domestic chick , 2004, Psychopharmacology.

[75]  E. Sellers,et al.  Attenuation of the euphoric effects of cocaine by the dopamine D1/D5 antagonist ecopipam (SCH 39166) , 1999, Archives of general psychiatry.

[76]  J. Panksepp The long-term psychobiological consequences of infant emotions: Prescriptions for the twenty-first century. , 2001 .

[77]  D. Self,et al.  Neural substrates of drug craving and relapse in drug addiction. , 1998, Annals of medicine.

[78]  E. Nestler,et al.  Molecular mechanisms of drug reinforcement and addiction. , 1995, Annual review of neuroscience.

[79]  J. Russell,et al.  Science Current Directions in Psychological the Structure of Current Affect : Controversies and Emerging Consensus on Behalf Of: Association for Psychological Science , 2022 .

[80]  P. Kalivas,et al.  Neuroadaptations involved in amphetamine and cocaine addiction. , 1998, Drug and alcohol dependence.

[81]  Brian Knutson,et al.  Anticipation of rewarding electrical brain stimulation evokes ultrasonic vocalization in rats. , 2000, Behavioral neuroscience.

[82]  T. Tonoue,et al.  Inhibition of shock-elicited ultrasonic vocalization by opioid peptides in the rat: A psychotropic effect , 1986, Psychoneuroendocrinology.

[83]  D. Landry,et al.  A catalytic antibody against cocaine prevents cocaine's reinforcing and toxic effects in rats. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[84]  A. Leshner Addiction is a brain disease, and it matters. , 1997, Science.

[85]  J. Panksepp,et al.  An autoradiographic map of (3H) diprenorphine binding in rat brain: Effects of social interaction , 1981, Brain Research Bulletin.

[86]  S. Brudzyński,et al.  High-frequency ultrasonic vocalization induced by intracerebral glutamate in rats , 1994, Pharmacology Biochemistry and Behavior.