James Olds and Pleasure in the Brain
OLDS, JAMES. Brain stimulation and the motivation of behavior.
Progress in Brain Research 45: 401-426, 1976.
Comment by Ralph Norgren (June, 2015)
Sixty years ago James Olds and Peter Milner brought pleasure into the brain with a paper entitled “Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain.” (Olds and Milner, 1954). The influence of this publication cannot be overstated. At minimum, it transformed our understanding of motivation, emotion, and reward, and influenced current conceptions of learning, mood disorders, addiction, and obesity.
At the time reward, or more commonly, reinforcement was central to psychological conceptions of learning. Although the hippocampus had been implicated in memory formation, the neuroscience of learning and reinforcement was largely theoretical (Hebb, 1948). What the Olds and Milner paper did was to place reward in the brain. It gave this psychological construct an anatomical substrate. Over the ensuing decades, the paradigm, intracranial self-stimulation, provided physiological access to this intervening variable. It made reward real.
In the public mind, this discovery quickly became associated with Olds and with the anatomical substrate for pleasure (Olds, 1956). Until then pleasure was more the realm of philosophy than science. The Swiss physiologist Walter R. Hess had explored the same brain areas as Olds using focal electrical stimulation in awake, behaving cats, an effort that contributed to his earning the Nobel Prize in 1949. As early as 1936, Erna and Frederic Gibbs reported that electrical stimulation of the brains of awake cats could elicit purring. After testing more than 400 sites throughout the brain, this response occurred at only 3, all in the posterior lateral hypothalamus. Twenty years later, Olds determined that in rats the same area supported self-stimulation at the highest rates and lowest thresholds of any site tested.
Why did Hess, the Gibbs, and others miss Olds’s discovery? They all used the same methodology and stimulated many of the same brain structures. Hess’s interest was in the central control of the autonomic nervous system. The Gibbs’s larger project was a study of convulsions. Both Hess and (Mr.) Gibbs trained as physicians and worked as physiologists. Neither their education nor their interests prepared them to recognize learning or reward.
Olds had an advantage; he was trained as an experimental psychologist. His Ph.D. dissertation involved operant learning in children under Richard Solomon at Harvard. He was thus was prepared to recognize learning. The same background meant that Olds had little if any experience with physiology or the brain. By the time he finished graduate training, however, he was convinced that understanding learning required brain research. That is why he chose postdoctoral study at The Montreal Neurological Institute under Donald Hebb.
Reward in the brain was discovered through a happy convergence of ineptitude and insight. Their initial objective was to implant electrodes in the midbrain reticular formation of rats and to study the behavioral effects of electrical stimulation there. Dr. Milner, three years older but still a graduate student, was assigned to teach Olds the routines needed to do the implants. After several demonstrations, Olds tried the surgery himself. Due to his inexperience with stereotaxic technique, in his first rat the electrode ended up well rostral in the forebrain rather than in the midbrain. They knew this because they had an X-ray of the skull. Before they finished testing this first animal, however, it died and they could not recover the brain for histology.
The original tests were conducted on an open field, a.k.a. a table top. The electrode was attached by thin wires to an AC step-down transformer through a rheostat. The line was interrupted by a switch. Once the rat had settled down, Olds periodically turned the switch ‘on’ and noted the animal’s behavior. He observed that if the switch was turned ‘on’ when the rat was in a distinct place on the table, say a corner, it was likely to return to that spot. The more often he turned the switch ‘on’ when the rat was in the same spot, the more frequently it returned there. Subsequently, he also determined that, if he changed the stimulation site on the table, the rat’s preference would change accordingly.
Olds recognized this effect as operant conditioning, and the electrical stimulation itself as the reinforcement. At the time, reinforcement was synonymous with reward, and reward meant pleasure. To legitimatize their observations to the learning community, they switched to testing the rat in a standard ’Skinner’ box in which the rewarded task was pressing a bar. [The laboratory did not own a Skinner box, so Milner built one.] It is these later results with a larger N that are presented in their classic paper.
Due to copyright issues, we were unable to post the Olds and Milner classic 1954 paper. To substitute, we have a 1976 review by Olds, published the year of his death, that provides an overview how he approached the problem of reward before and after this seminal discovery.
Note on sources: This story relies primarily on five sources – the publication itself, a short paper by Olds in Scientific American, a biographical sketch of Dr. Olds by Dr. Richard F. Thompson, an autobiographical note by Dr. Peter M. Milner, and my recollections of recountings by Dr. Olds while I was a graduate student in his laboratory (1965–1969). Although self-stimulation research was still going on in his lab, during my years there Olds’s day-to-day attention was focused on the neural bases of learning by recording single unit activity in awake, behaving rats using fine-wire electrodes. Olds championed this approach for years before it was accepted by the neurophysiologists of the day. The technique eventually provided the technological basis for the 2014 Nobel Prize in Physiology and Medicine, but that is another story.
Gibbs EL, Gibbs FA. A purring center in the brain. J. Comp. Neurol. 64: 209-211, 1936.
Hebb DO. The Organization of Behavior. New York: J. H. Wiley & Sons, 1949, 1961.
Hess WR. The Functional Organization of the Diencephalon (edited by J. R. Hughes; transl. by P. V. Deporte). New York: Grune, 1958.
Milner PM. ‘Peter Milner’ in The History of Neuroscience, Vol. 8, http://www.sfn.org/~/media/SfN/Documents/TheHistoryofNeuroscience/Volume%208/PeterMilner.ashx (Referenced 28 April 2015).
Olds J. Pleasure centers in the brain. Sci. Am. 1956, 195:105-116.
Olds J. Brain stimulation and the motivation of behavior. Prog Brain Res. 1976, 45: 401-426.
Olds J, Milner PM. Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. J. Comp. Physiol. Psychol. 1954, 47: 419 - 427.
Thompson RF. ‘James Olds’ in Biographical Memoirs 77: 1-19, Washington, D.C., National Academy of Sciences Press, 1999. http://www.nasonline.org/publications/biographical-memoirs/memoir-pdfs/olds-james.pdf