Abstract

Dopaminergic neurons contribute to intracranial self-stimulation (ICSS) and other reward-seeking behaviors, but it is not yet known where dopaminergic neurons intervene in the neural circuitry underlying reward pursuit or which psychological processes are involved. In rats working for electrical stimulation of the medial forebrain bundle, we assessed the effect of GBR-12909, a specific blocker of the dopamine transporter. Operant performance was measured as a function of the strength and cost of electrical stimulation. GBR-12909 increased the opportunity cost most subjects were willing to pay for a reward of a given intensity. However, this effect was smaller than that produced by a regimen of cocaine administration that drove similar increases in nucleus accumbens (NAc) dopamine levels in unstimulated rats. Delivery of rewarding stimulation to drug-treated rats caused an additional increase in dopamine concentration in the NAc shell in cocaine-treated, but not GBR-treated, rats. These behavioral and neurochemical differences may reflect blockade of the norepinephrine transporter by cocaine but not by GBR-12909. Whereas the effect of psychomotor stimulants on ICSS has long been attributed to dopaminergic action at early stages of the reward pathway, the results reported here imply that increased dopamine tone boosts reward pursuit by acting at or beyond the output of the circuitry that temporally and spatially summates the output of the directly stimulated neurons underlying ICSS. The observed enhancement of reward seeking could be due to a decrease in the value of competing behaviors, a decrease in subjective effort costs, or an increase in reward-system gain.

Video:
The video reveals a fundamental source of ambiguity in two-dimensional measurements of operant performance for reward, such as those obtained in the curveshift and progressive-ratio paradigms. We show how the three-dimensional portrayal provided by the reward-mountain model resolves this ambiguity. The reward-mountain model is derived, described, discussed, and applied in the following papers:

• Arvanitogiannis A, & Shizgal P (2008). The reinforcement mountain: allocation of behavior as a function of the rate and intensity of rewarding brain stimulation. Behav Neurosci 122:1126-1138. doi: 10.1037/a0012679
http://psycnet.apa.org/journals/bne/122/5/1126/

• Hernandez G, Breton YA, Conover K, & Shizgal P (2010). At what stage of neural processing does cocaine act to boost pursuit of rewards? PLoS One 5:e15081. doi: 10.1371/journal.pone.0015081
http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0015081

• Shizgal, P, & Hernandez, G (2010). Intracranial Self-Stimulation. Encyclopedia of Psychopharmacology, 653–660. doi:10.1007/978-3-540-68706-1_66
http://www.springerlink.com/content/w37074k2586301j6/?MUD=MP

• Trujillo-Pisanty I, Hernandez G, Moreau-Debord I, Cossette MP, Conover K, Cheer JF, & Shizgal P (2011). Cannabinoid receptor blockade reduces the opportunity cost at which rats maintain operant performance for rewarding brain stimulation. J Neurosci 31:5426-5435.
http://www.jneurosci.org/content/31/14/5426.long

• Shizgal, P. (2012). Scarce means with alternative uses: Robbins' definition of economics and its extension to the behavioral and neurobiological study of animal decision making. Frontiers in Neuroscience, 6, 20. doi:10.3389/fnins.2012.00020
http://www.frontiersin.org/Decision_Neuroscience/10.3389/fnins.2012.00020/abstract

• Hernandez, G., Trujillo-Pisanty, I., Cossette, M-P., Conover, K., & Shizgal, P. (2012). Role of dopamine tone in the pursuit of brain stimulation reward. Journal of Neuroscience, 2012, in press.