Neuroregulators and the reinforcement of smoking: Towards a biobehavioral explanation

https://doi.org/10.1016/0149-7634(84)90007-1Get rights and content

Abstract

This paper examines findings on the neuroregulatory effects of nicotine in an effort to formulate a unified hypothesis that can explain the remarkable persistence of smoking behavior. Because nicotine alters the bioavailability of several behaviorally active neuroregulators, including acetylcholine, norepinephrine, dopamine, beta-endorphin, and vasopressin, we propose that nicotine is “used” by smokers to produce temporary improvements in performance or affect. Under this formulation, a potentially large number of exteroceptive and interoceptive cues unrelated to the nicotine-dependence cycle may serve as discriminative stimuli for smoking, over and above smoking to terminate or avoid withdrawal. The rapid action of nicotine, and its diverse neuroregulatory effects, render it particularly effective as a “coping response” to the demands of daily living. Of special interest in this regard is a biphasic pattern of arousal/alertness during smoking followed by calming/tension-reduction after smoking, which may result from cholinergic/catecholaminergic activation followed by cholinergic blockade or betaendorphin release. Apparently smokers can adjust nicotine intake to enhance these effects selectively, which may add considerably to the appeal of smoking.

References (174)

  • G.H. Hall et al.

    Effects of nicotine on the release of 3H-noradrenaline from the hypothalamus

    Biochem Pharmacol

    (1972)
  • J.E. Henningfield et al.

    Control of behavior by intravenous nicotine injections in human subjects

    Pharmacol Biochem Behav

    (1983)
  • J.E. Henningfield et al.

    Nicotine as a reinforcer in human subjects and laboratory animals

    Pharmacol Biochem Behav

    (1983)
  • R.G. Hill

    The status of naloxone in the identification of pain control mechanisms operated by endogenous opioids

    Neurosci Lett

    (1981)
  • S.G. Kamerling et al.

    Interaction between nicotine and endogenous opioid mechanisms in the unanesthetized dog

    Pharmacol Biochem Behav

    (1982)
  • A. Karras et al.

    Naloxone reduces cigarette smoking

    Life Sci

    (1980)
  • J.J. Legros et al.

    Influence of vasopressin on learning and memory

    Lancet

    (1978)
  • S.I. Mason et al.

    Theories of the dorsal bundle extinction effect

    Brain Res Rev

    (1979)
  • M.F. McCarty

    Nutritional support of central catecholaminergic tone may aid smoking withdrawal

    Med Hypotheses

    (1982)
  • E.L. Abel

    Drugs and Behaviour

    (1974)
  • G. Ainslie

    Specious reward: A behavioral theory of impulsiveness and impulse control

    Psychol Bull

    (1975)
  • K. Andersson

    Effects of cigarette smoking on learning and retention

    Psychopharmacologia

    (1975)
  • K. Andersson et al.

    Effects of acute central and peripheral administration of nicotine on hypothalamic catecholamine nerve terminal systems and on the secretion of adenohypophyseal hormones in the male rat

    Med Biol

    (1982)
  • A.K. Armitage et al.

    Absorption and metabolism of nicotine from cigarettes

    Br Med J

    (1975)
  • H. Ashton et al.

    The use of event-related slow potentials of the brain in the analysis of the effects of cigarette smoking and nicotine in humans

  • H. Ashton et al.

    Smoking: Psychology and Pharmacology

    (1982)
  • D.J.K. Balfour

    The pharmacology of nicotine dependence: A working hypothesis

    Pharm Ther

    (1982)
  • K. Bättig

    The smoking habit and psychopharmacological effects of nicotine

    Activitas Nervosa Superior

    (1980)
  • B.D. Berger et al.

    An analysis of the learning deficits produced by scopolamine

    Psychopharmacologia

    (1969)
  • R.M. Bergland et al.

    Can the pituitary secrete directly to the brain? (Affirmative anatomical evidence)

    Endocrinology

    (1978)
  • G.W. Bisset et al.

    Vasopressin release by nicotine: The site of action

    Br J Pharmacol

    (1975)
  • M.A. Bozarth

    Opiate reward mechanisms mapped by intracranial self-administration

  • M.A. Bozarth et al.

    Anatomically distinct opiate receptor fields mediate reward and physical dependence

    Science

    (1984)
  • M.B. Carpenter et al.

    Human Neuroanatomy

  • D.B. Carr et al.

    Endotoxin-stimulated opioid peptide secretion: Two secretory pools and feedback control in vivo

    Science

    (1982)
  • M. Carruthers

    Modification of the noradrenaline related effects of smoking by beta-blockade

    Psychol Med

    (1976)
  • E.M. Castro de Souza et al.

    The release of vasopressin by nicotine: Further studies on its site of action

    J Physiol

    (1977)
  • D.R. Cherek

    Effects of smoking different doses of nicotine on human aggressive behavior

    Psychopharmacology (Berlin)

    (1981)
  • P.E. Cryer et al.

    Norepinephrine and epinephrine release and adrenergic mediation of smoking-associated hemodynamic and metabolic events

    N Engl J Med

    (1976)
  • K.L. Davis et al.

    Cholinergic underactivity in human memory disorders

    Life Sci

    (1978)
  • W.M. Davis et al.

    Blocking effect of alpha-methyltyrosine on amphetamine-based reinforcement

    J Pharm Pharmacol

    (1973)
  • G.A. Deneau et al.

    Self-administration of psychoactive substances by the monkey

    Psychopharmacologia

    (1969)
  • E.F. Domino

    Behavioral, electrophysiological, endocrine, and skeletal muscle actions of nicotine and tobacco smoking

  • E.F. Domino

    Neuropsychopharmacology of nicotine and tobacco smoking

  • L. Epstein et al.

    The measurement of situational influences of smoking

    Addict Behav

    (1977)
  • D. Evans et al.

    Long-term outcome of smoking cessation workshops

    Am J Public Health

    (1980)
  • J.L. Falk et al.

    Commonalities in the environmental control of behavior

  • C. Feyerabend et al.

    Effects of urinary pH and nicotine excretion rate on plasma nicotine during cigarette smoking and chewing nicotine gum

    Br J Clin Pharmacol

    (1978)
  • J. Fleming et al.

    The effects of nicotine on two-way avoidance conditioning in bidirectionally selected strains of rats

    Psychopharmacologia

    (1975)
  • Cited by (326)

    • Examination of the Gateway Hypothesis in a rat model

      2019, Pharmacology Biochemistry and Behavior
      Citation Excerpt :

      Rats were anesthetized with a ketamine/xylazine (100 mg/kg and 10 mg/kg) IP solution. Catheters were implanted in the jugular vein following procedures described previously (Pomerleau and Pomerleau, 1984; Thomsen and Caine, 2005). Rats were observed during recovery from surgery until the anesthesia wore off and they were ambulatory.

    View all citing articles on Scopus
    View full text