Elsevier

Brain Research

Volume 73, Issue 3, 28 June 1974, Pages 381-419
Brain Research

Catecholamine systems as the neural substrate for intracranial self-stimulation: a hypothesis

https://doi.org/10.1016/0006-8993(74)90666-0Get rights and content

Abstract

The hypothesis was investigated that activation of central catecholamine (CA) systems is essential for intracranial self-stimulation (ICSS). Brain sites that support ICSS in the rat were found to be highly correlated with electrodes in 3 major CA systems: the mesolimbic and nigrostriatal dopaminergic systems and the dorsal noradrenergic system. Stimulation at ICSS loci in the brain stem causes release of catecholamines at terminals in ascending CA systems. Lesion studies show suppression of ICSS proportional to the degree of damage to the stimulated CA system. Drugs influence ICSS in accordance with their effects on transmission at dopaminergic and noradrenergic synapses. Enhancement of nicotinic-cholinergic mechanisms facilitates ICSS, but the effect requires that CA mechanisms be intact. Neurophysiological experiments suggest that two systems characterized by different axonal refractory periods are involved in ICSS. The data are insufficient to determine whether these correspond to the dopamine and norepinephrine systems. Norepinephrine has an inhibitory effect at many postsynaptic receptor sites, and ICSS is often accompanied by reduction or cessation of cellular discharges in NE terminal areas. Food ingestion has also been demonstrated to produce an inhibitory effect on cells in a noradrenergic terminal area.

ICSS has been demonstrated in numerous species, including man, in brain areas that overlap considerably with loci whose stimulation supports ICSS in the rat. Stimulation of ICSS loci in man is commonly associated with verbal reports of intense pleasurable sensations.

Reference (211)

  • CrowT.J. et al.

    Intracranial self-stimulation with electrodes in the region of the locus coeruleus

    Brain Research

    (1972)
  • DescarriesL. et al.

    Disappearance of the locus coeruleus in the rat after intraventricular 6-hydroxydopamine

    Brain Research

    (1972)
  • GermanD.C. et al.

    Behaviorally determined neurophysiological properties of MFB self-stimulation fibers

    Physiol. Behav.

    (1972)
  • GibsonS. et al.

    Effect of selective inhibitors of tyrosine and tryptophan hydroxylases on self-stimulation in the rat

    Exp. Neurol.

    (1970)
  • GoodmanI.J. et al.

    Stimulation of positively and negatively reinforcing sites in the avian brain

    Life Sci.

    (1966)
  • HofferB.J. et al.

    Studies on norepinephrine-containing afferents to purkinje cells of rat cerebellum. II. Sensitivity of purkinje cells to norepinephrine and related substances administered by microiontophoresis

    Brain Research

    (1971)
  • HustonJ.P. et al.

    Operant conditioning in forebrain ablated rats by use of rewarding hypothalamic stimulation

    Brain Research

    (1973)
  • KatzmanR. et al.

    Evidence for regenerative axon sprouting of central catecholamine neurons in the rat mesencephalon following electrolytic lesions

    Brain Research

    (1971)
  • KeeneJ.J. et al.

    Excitatory connection from lateral hypothalamic self-stimulation sites to escape sites in medullary reticular formation

    Exp. Neurol.

    (1970)
  • KeeneJ.J. et al.

    Rewarding and aversive brain stimulation opposite effects on medial thalamic units

    Physiol. Behav.

    (1973)
  • La VailJ.H. et al.

    A method based on retrograde intra-axonal transport of protein for identification of cell bodies of origin of axons terminating within the CNS

    Brain Research

    (1973)
  • LiebmanJ.M. et al.

    Self-stimulation loci in the midbrain central gray matter of the rat

    Behav. Biol.

    (1973)
  • LoizouL.A.

    Projections of the nucleus locus coeruleus in the albino rat

    Brain Research

    (1969)
  • LorensS.A.

    Affect of lesions in the raphe system of self-stimulation in the rat

    Physiol. Behav.

    (1971)
  • MadrygaF.J. et al.

    Procaine injections into MFB-LHA during septal and preoptic self-stimulation

    Physiol. Behav.

    (1971)
  • MaedaT. et al.

    Projections ascendantes du locus coeruleus et d'autres neurones aminergiques au niveau du prosence´phale du rat

    Brain Research

    (1972)
  • AdametzJ.H.

    Rate of recovery of functioning in cats with rostral reticular lesions

    J. Neurosurg.

    (1959)
  • AnandB.K. et al.

    Hypothalamic control of food intake in rats and cats

    Yale J. Biol. Med.

    (1951)
  • AndrewsR.J.

    Intracranial self-stimulation in the chick

    Nature (Lond.)

    (1967)
  • AndyO.J.

    General discussion following Chapters 33–35

  • AnnauZ. et al.

    Effects of prolonged water deprivation on hypothalamic self-stimulation

    Amer. J. Physiol.

    (1971)
  • AtrensD.M.

    A reinforcement analysis of rat hypothalamus

    Amer. J. Physiol.

    (1973)
  • Benesˇova´O.

    The action of cocaine, atropine, and tricyclic antidepressants on self-stimulation in rats

  • BishopM.P. et al.

    Intracranial self-stimulation in man

    Science

    (1963)
  • BlackW.C. et al.

    Reduction of electrically-rewarded behavior by interference with monoamine synthesis

    Physiol. Behav.

    (1970)
  • BloomF.E. et al.

    Physiologic and pharmacologic considerations of biogenic amines in the nervous system

    Ann. Rev. Pharmacol.

    (1968)
  • BowerG.H. et al.

    Rewarding and punishing effects from stimulating the same place in the rat's brain

    J. comp. physiol. Psychol.

    (1958)
  • BoydE.S. et al.

    Effect of some brain lesions on septal intracranial self-stimulation in the rat

    Amer. J. Physiol.

    (1970)
  • BoydE.S. et al.

    Positive and negative reinforcement from intracranial self-stimulation in teleosts

    Science

    (1962)
  • BoydE.S. et al.

    Effect of some brain lesions on intracranial self-stimulation in the rat

    Amer. J. Physiol.

    (1967)
  • BradyJ.V.

    Temporal and emotional factors related to electrical self-stimulation of the limbic system

  • BradyJ.V.

    Temporal and emotional effects related to intracranial electrical self-stimulation

  • BradyJ.V. et al.

    Some effects of brain stimulation on timing behavior

    J. exp. Anal. Behav.

    (1960)
  • BreeseG.R. et al.

    Effect of 6-hydroxydopamine on electrical self stimulation of the brain

    Brit. J. Pharmacol.

    (1971)
  • BreeseG.R. et al.

    Effect of 6-hydroxydopamine on brain norepinephrine and dopamine: evidence for selective degeneration of catecholamine neurons

    J. Pharmacol. exp. Ther.

    (1970)
  • BrunerA.

    Self-stimulation in the rabbit: an anatomical map of stimulation effects

    J. comp. Neurol.

    (1967)
  • BurkardW.P. et al.

    Effect of 6-hydroxydopamine on behavior and cerebral amine content in rats

    Experientia (Basel)

    (1969)
  • BurstenB. et al.

    Positive reinforcement induced by intracranial stimulation in the monkey

    J. comp. physiol. Psychol.

    (1958)
  • CaseyK.L. et al.

    Unit analysis of the effects of motivating stimuli in the awake animal: pain and self-stimulation

  • ChuN. et al.

    Norepinephrine-containing neurons: changes in spontaneous discharge patterns during sleeping and waking

    Science

    (1973)
  • Cited by (295)

    • Reward processing in food addiction and overeating

      2019, Compulsive Eating Behavior and Food Addiction: Emerging Pathological Constructs
    • Methamphetamine modulates glutamatergic synaptic transmission in rat primary cultured hippocampal neurons

      2014, Brain Research
      Citation Excerpt :

      Elevating GLU synaptic transmission in local circuitry and changes in the electrophysiological properties of neurons involved in the reward circuit seem to be of utmost importance in addiction (Ernst et al., 2000). The hippocampus is a particularly suitable structure for studying the role of psychostimulants in light of its exceptional monoaminergic innervation and its support of ICSS (Ursin et al., 1966; German and Bowden, 1974). The hippocampus has a significant site for drug reward/reinforcement, most likely due to its anatomical circuit to the VTA via the NAc and VP (Lisman and Grace, 2005).

    • Dual roles of dopamine in food and drug seeking: The drive-reward paradox

      2013, Biological Psychiatry
      Citation Excerpt :

      That subsystems might serve different functions is suggested, first, by the nominal differentiation of nigrostriatal, mesolimbic, and mesocortical systems and by subsystems within them. The nigrostriatal system is traditionally associated with the initiation of movement, whereas the mesolimbic system is more traditionally associated with reward (89,90) and motivational (91) function (but see [92]). The mesocortical system is also implicated in reward function (93–95).

    • Fight, flight, or fall: Autonomic nervous system reactivity during skydiving

      2012, Personality and Individual Differences
      Citation Excerpt :

      ANS activation leads to rapid increases in HR and release of epinephrine, which would typically aid an individual in fighting or running from a threat (Kemeny, 2003); however, if the individual does not perceive the stressor as threatening, ANS activation, and the subsequent release of epinephrine, may be interpreted as pleasant and rewarding. In fact, the release of epinephrine and norepinepherine associated with ANS activation may modulate the reward system in the brain (German & Bowden, 1974). The lack of habituation in this system may be the mechanism leading individuals to engage in the behavior repeatedly as they attempt to achieve activation of the ANS.

    View all citing articles on Scopus
    View full text