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Cannabinoid Conditioned Reward and Aversion: Behavioral and Neural Processes Jennifer E University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications, Department of Psychology Psychology, Department of 2010 Cannabinoid Conditioned Reward and Aversion: Behavioral and Neural Processes Jennifer E. Murray University of Nebraska-Lincoln, [email protected] Rick A. Bevins University of Nebraska-Lincoln, [email protected] Follow this and additional works at: http://digitalcommons.unl.edu/psychfacpub Part of the Psychology Commons Murray, Jennifer E. and Bevins, Rick A., "Cannabinoid Conditioned Reward and Aversion: Behavioral and Neural Processes" (2010). Faculty Publications, Department of Psychology. 730. http://digitalcommons.unl.edu/psychfacpub/730 This Article is brought to you for free and open access by the Psychology, Department of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications, Department of Psychology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. pubs.acs.org/acschemicalneuroscience Review Cannabinoid Conditioned Reward and Aversion: Behavioral and Neural Processes Jennifer E. Murray*,†,‡ and Rick A. Bevins† †Department of Psychology, University of Nebraska;Lincoln, Lincoln, Nebraska, and ‡Department of Experimental Psychology, University of Cambridge, Cambridge, U.K. Abstract 1. Introductory remarks solation of brain cannabinoid (CB) receptors and the endogenous CB compounds, arachidonyletha- I nolamide (anandamide) and 2-arachidonylglycerol (2-AG), as well as the development of exogenous ligands, has enabled a growing body of research into the actions of cannabinoids in the brain and their effects on behavior. Because the primary active ingredient of marijuana is cannabinoidergic and because the prevalence of marijua- na use is a global concern, an area of particular interest is how the CB system functions within the brain reward The discovery that delta-9-tetrahydrocannabinol system. Place conditioning is a common and potentially (Δ9-THC) is the primary psychoactive ingredient in useful task for evaluating the conditioned motivational marijuana prompted research that helped elucidate effects of a drug (1, 2). In this task, the animal (usually a the endogenous cannabinoid system of the brain. rat or mouse) has a distinct environment (context) Δ9-THC and other cannabinoid ligands with agonist repeatedly paired with the drug of interest. There is an action (CP 55,940, HU210, and WIN 55,212-2) alternate environment that differs along some stimulus increase firing of dopamine neurons and increase dimension(s) that is equally experienced, but not paired synaptic dopamine in brain regions associated with with the drug. Using this method of Pavlovian condition- reward and drug addiction. Such changes in cellular ing, the conditioned appetitive (rewarding) or aversive processes have prompted investigators to examine effects of a drug can be assessed. A conditioned place the conditioned rewarding effects of the cannabinoid preference (CPP) is inferred when in a choice test animals ligands using the place conditioning task with rats and spend more time in an environment that had been mice. As reviewed here, these cannabinoid ligands previously paired with a drug stimulus compared to an can condition place preferences (evidence for rewar- alternate environment. Such an outcome suggests that ding effects) and place aversions (evidence for aver- the drug has some rewarding effects that entered into an sive qualities). Notably, the procedural details used association with the paired environment. A conditioned in these place conditioning studies have varied across place aversion (CPA) is inferred when animals spend less laboratories. Such variation includes differences time in the drug-paired environment; this outcome is in apparatus type, existence of procedural biases, taken to indicate an aversive effect of the drug (see later dose, number of conditioning trials, injection- for more detailed discussion). to-placement intervals, and pretraining drug expo- Similar to other behavioral research, the parameters sure. Some differences in outcome across studies can used in place conditioning studies with CB ligands be explained by these procedural variables. For vary widely across laboratories. With some drugs, example, low doses of Δ9-THC appear to have con- these variations in procedural details across labora- ditioned rewarding effects, whereas higher doses tories seem to make little difference in the overall have aversive effects that either mask these reward- conclusion regarding the motivational impact of the ing effects or condition a place aversion. Throughout drug. As detailed in Tzschentke’s (3) excellent review this review, we highlight key areas that need further of the place conditioning literature, studies with drugs research. such as cocaine or amphetamine consistently report CPP. The opiate drug heroin produces CPP, whereas Keywords: Drug addiction, choice behavior, conditioned place preference, marijuana, mesolimbic dopamine, Received Date: January 21, 2010 reward Accepted Date: February 16, 2010 Published on Web Date: March 10, 2010 r 2010 American Chemical Society 265 DOI: 10.1021/cn100005p |ACS Chem. Neurosci. (2010), 1, 265–278 pubs.acs.org/acschemicalneuroscience Review the opioid antagonist naloxone consistently produces anterior part of the medial forebrain bundle, the cingu- CPA. Alternatively, place conditioning literature in- late cortex, amygdala, claustrum, and nucleus accum- volving the cannabinoid system seems to parallel the bens were found in moderate density. Finally, CB1 place conditioning literature with nicotine. That is, receptors were found in low density in the thalamus, reports of no effect, CPA, and CPP with no clear hypothalamus, periaqueductal gray, pons, medulla, answer yet as to the relevant conditions under which and the area postrema. conditioned appetitive or aversive effects will be ex- Importantly, receptor density does not necessarily pressed. With this in mind, the purpose of the present indicate signaling strength. CB receptors are G-protein review was to discuss the role of cannabinoids within coupled (13), meaning the effects of receptor binding are the reward (motivation) system and to coalesce into mediated by the second messenger pathways activated one paper the published research on place condition- by the G-protein. As such, binding can have a different ing with cannabinoid agonists. In doing so, we hoped impact depending on localization. For instance, using to identify some critical variables that predict when a autoradiography and membrane saturation analyses in cannabinoid agonist may have conditioned appetitive male Sprague-Dawley rats, the average number of versus conditioned aversive effect. Such information G-proteins activated per bound CB1 receptor (i.e., would be important for guiding future research at- amplification factor) was lowest in the frontal cortex, tempting to identify the behavioral and neurochemical cerebellum, hippocampus, and striatum (14). These are processes underlying the conditioned motivational regions with generally high numbers of receptors. Mode- effects of cannabinoid agonists. rate amplification factors were found in the thalamus, brainstem, amygdala, and sensorimotor cortex. Finally, 2. Endogenous Cannabinoid System the hypothalamus had the highest amplification factor, an area with low receptor density. These data suggest 2.1. Receptors that areas with low receptor density may enhance signal Cannabis has been used for thousands of years for its strength by increasing the impact of G-proteins on mood-altering, hallucinogenic, and anesthetic proper- subsequent intracellular processes. ties. The neurological effects of the drug suggested a The location of these receptors on neurons is impor- central mechanism of action. Delta-9-tetrahydrocanna- Δ9 tant for understanding receptor function. CB1 receptors binol ( -THC) was isolated as the primary psycho- have been found to be primarily localized presynapti- active component of cannabis (4). This compound was cally on GABAergic neurons as determined by electro- then used to help elucidate the CB receptors (5). CB physiological analyses (15, 16). This presynaptic receptors have been divided into two groups, CB1 and localization suggests a modulatory role of endocan- CB2 receptors, on the basis of functionality and distri- nabinoids. Notably, G-protein activation by bound bution. CB1 receptors are found widely throughout the 2þ CB1 receptors reduces Ca conductance (17)and brain and perform a variety of modulatory functions, increases Kþ conductance (18). Both of these actions whereas the CB2 receptors have generally been asso- have been linked to a process known as depolariza- ciated with the peripheral and central regulation of the tion-induced suppression of inhibition (19). As dia- immune system (6, 7, 8). Furthermore, recent evidence gramed in Figure 1, activation of presynaptic CB1 suggests non-CB receptor binding of endogenous receptors functions to inhibit subsequent neuro- (internally produced) and exogenous (externally transmitter release from that presynaptic terminal produced) cannabinoid compounds (9, 10). The current (20). Postsynaptic endogenous cannabinoid release review will primarily focus on the CB1 receptor because increases with increased postsynaptic excitation [(21) of its purported role involving the rewarding and re- see later]. The subsequent retrograde cannabinoid inforcing effects of drugs. signaling can attenuate the release
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