Serotonergic mechanisms promote dominance acquisition in adult male vervet monkeys

In a counter-balanced, cross-over study, we examined the contributions of serotonergic systems to the acquisition of social dominance in adult male vervet monkeys. Subjects were members of 12 social groups, each containing 3 adult males, at least 3 adult females, and their offspring. Animals were observed in 5 intervals including a first baseline, a first experimental, a second baseline, a second experimental, and a third baseline period. At the end of the first baseline period, the dominant male was removed from each group. In each group, one of the two remaining subordinate males was selected at random for treatment and during the first experimental period, 6 of the 12 treated males received drugs that enhanced serotonergic activity (3 were given tryptophan 40 mg/kg/day and 3 fluoxetine 2 mg/kg/day). The other 6 treated males received drugs that reduced serotonergic function (3 were given fenfluramine 2 mg/kg/day and 3 cyproheptadine 60 micrograms/kg/day). At the end of the first experimental period, the original dominant male was returned to his group and the second baseline period began. In all instances, the originally dominant male regained his dominant position. The second experimental period began with the dominant male again being removed and, the 12 treated males were given the treatment they had not received in the first experimental period. At the start of the third 12-week baseline period, the original dominant male was returned to his group and resumed his dominant status. When the 12 treated subjects received tryptophan or fluoxetine, they became dominant in all instances. When they received fenfluramine or cyproheptadine, their vehicle-treated cage mates became dominant. The sequence of the behavioral changes shown by the treated males as they acquired dominance status paralleled those seen in naturalistic conditions. These observations support the distinction between dominance and aggression and strongly suggest that when hierarchical relationships are uncertain, serotonergic mechanisms may mediate the behaviors which permit a male to attain high dominance status.

[1]  M. Linnoila,et al.  Cerebrospinal fluid monoamine metabolites and suicidal behavior in depressed patients. A 5-year follow-up study. , 1989, Archives of general psychiatry.

[2]  F. Waal Class structure in a rhesus monkey group: the interplay between dominance and tolerance , 1986, Animal Behaviour.

[3]  E. sanders-Bush The Serotonin Receptors , 1989, The Receptors.

[4]  A. Harcourt,et al.  Alliances in contests and social intelligence. , 1988 .

[5]  M. Raleigh,et al.  Adaptation, selection, and benefit-cost balances: Implications of behavioral-physiological studies of social dominance in male vervet monkeys , 1984 .

[6]  K. E. Moore,et al.  Exogenous Tryptophan Increases Synthesis, Storage, and Intraneuronal Metabolism of 5‐Hydroxytryptamine in the Rat Hypothalamus , 1986, Journal of neurochemistry.

[7]  R. Mailman,et al.  Long-term effects of early social isolation in Macaca mulatta: changes in dopamine receptor function following apomorphine challenge , 1990, Brain Research.

[8]  D. Cheney Interactions and relationships between groups , 1987 .

[9]  J. Altmann,et al.  Observational study of behavior: sampling methods. , 1974, Behaviour.

[10]  F. Waal,et al.  The Integration of Dominance and Social Bonding in Primates , 1986, The Quarterly Review of Biology.

[11]  M. Raleigh,et al.  Serotonergic influences on the social behavior of vervet monkeys (Cercopithecus aethiops sabaeus) , 1980, Experimental Neurology.

[12]  S. Young,et al.  Tryptophan availability, 5ht synthesis and 5HT function , 1989, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[13]  Myers Re Role of prefrontal and anterior temporal cortex in social behavior and affect in monkeys. , 1972 .

[14]  H. D. Steklis,et al.  Effects of orbitofrontal and temporal neocortical lesions on the affiliative behavior of vervet monkeys (Cercopithecus aethiops sabaeus) , 1981, Experimental Neurology.

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

[16]  B. Adinoff,et al.  Acting out hostility in normal volunteers: Negative correlation with levels of 5HIAA in cerebrospinal fluid , 1988, Psychiatry Research.

[17]  Cloninger Cr A systematic method for clinical description and classification of personality variants: A proposal. , 1987 .

[18]  M. Raleigh,et al.  Social dominance in adult male vervet monkeys: Behavior-biochemical relationships , 1983 .

[19]  Michael P. Johnson,et al.  Comparative serotonin neurotoxicity of the stereoisomers of fenfluramine and norfenfluramine , 1990, Pharmacology Biochemistry and Behavior.

[20]  R. Pihl,et al.  The effect of altered tryptophan levels on mood and behavior in normal human males. , 1986, Clinical neuropharmacology.

[21]  P. Cowen Neuroendocrine Responses to Tryptophan as an Index of Brain Serotonin Function , 1988 .

[22]  T. Struhsaker Behavior of vervet monkeys (Cercopithecus aethiops) , 1967 .

[23]  Douglas Madsen Power Seekers are Different: Further Biochemical Evidence , 1986, American Political Science Review.

[24]  G. Kraemer,et al.  A longitudinal study of the effect of different social rearing conditions on cerebrospinal fluid norepinephrine and biogenic amine metabolites in rhesus monkeys. , 1989, Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology.

[25]  J. R. Walters Conflict and Cooperation , 2018, The Essence of Politics.

[26]  R. Seyfarth,et al.  How Monkeys See the World: Inside the Mind of Another Species , 1990 .

[27]  D. Eccleston,et al.  THE EFFECTS OF PRECURSOR LOADING IN THE CEREBRAL METABOLISM OF 5‐HYDROXYINDOLES , 1968, Journal of neurochemistry.

[28]  L. Fedigan Dominance and reproductive success in primates , 1983 .

[29]  D. Wong,et al.  Fluoxetine and its two enantiomers as selective serotonin uptake inhibitors. , 1990, Acta pharmaceutica Nordica.

[30]  R. Sapolsky Adrenocortical function, social rank, and personality among wild baboons , 1990, Biological Psychiatry.

[31]  B. Chapais Rank Maintenance in Female Japanese Macaques: Experimental Evidence for Social Dependency , 1988 .

[32]  J. Contrera,et al.  Effects of high‐dose fenfluramine treatment on monoamine uptake sites in rat brain: Assessment using quantitative autoradiography , 1990, Synapse.

[33]  A. Kling,et al.  Social Behavior of Monkeys Selectively Depleted of Monoamines , 1971, Science.

[34]  5-Hydroxytryptamine receptor subtypes. , 1990, Pharmacology & toxicology.

[35]  M. Raleigh,et al.  Behavioral and Cognitive Effects of Altered Tryptophan and Tyrosine Supply , 1988 .

[36]  M. Raleigh,et al.  Female influnces on male dominance acquisition in captive vervet monkeys, Cercopithecus aethiops sabaeus , 1989, Animal Behaviour.

[37]  W. Pardridge Brain metabolism: a perspective from the blood-brain barrier. , 1983, Physiological reviews.

[38]  B. J. Winer Statistical Principles in Experimental Design , 1992 .

[39]  C. Snowdon,et al.  Reproductive performance and excretion of urinary estrogens and gonadotropins in the female pygmy marmoset (Cebuella pygmaea) , 1990, American journal of primatology.

[40]  M. Raleigh,et al.  Dominant social status facilitates the behavioral effects of serotonergic agonists , 1985, Brain Research.

[41]  J. Silk,et al.  Continuity and change in dominance relations among female baboons , 1987, Animal Behaviour.

[42]  R. Wurtman,et al.  Effects of their nutrient precursors on the synthesis and release of serotonin, the catecholamines, and acetylcholine: implications for behavioral disorders. , 1988, Clinical neuropharmacology.

[43]  K. Miczek,et al.  Brain 5-HT and inhibition of aggressive behavior in animals: 5-HIAA and receptor subtypes. , 1989, Psychopharmacology bulletin.

[44]  M. Weissman,et al.  The hidden patient: unrecognized panic disorder. , 1990, The Journal of clinical psychiatry.

[45]  S. Peroutka,et al.  Neurochemistry and neurotoxicity of substituted amphetamines. , 1990, Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology.

[46]  H. D. Steklis,et al.  A neural substrate for affiliative behavior in nonhuman primates. , 1976, Brain, behavior and evolution.

[47]  J. Contrera,et al.  Effects of repeated fenfluramine administration on indices of monoamine function in rat brain: pharmacokinetic, dose response, regional specificity and time course data. , 1990, The Journal of pharmacology and experimental therapeutics.

[48]  S. Peroutka,et al.  Serotonin receptor and reuptake sites: pharmacologic significance. , 1990, The Journal of clinical psychiatry.

[49]  S. Siegel,et al.  Nonparametric Statistics for the Behavioral Sciences , 2022, The SAGE Encyclopedia of Research Design.

[50]  F. Bercovitch,et al.  Coalitions, cooperation and reproductive tactics among adult male baboons , 1988, Animal Behaviour.