Bilateral lesions of the thalamic trigeminal orosensory area dissociate natural from drug reward in contrast paradigms.

Abstract

Substance abuse and addiction are associated with an apparent devaluation of, and inattention to, natural rewards. This consequence of addiction can be modeled using a reward comparison paradigm where rats avoid intake of a palatable taste cue that comes to predict access to a drug of abuse. Evidence suggests rats avoid intake following such pairings, at least in part, because the taste cue pales in comparison to the highly rewarding drug expected in the near future. In accordance, lesions of the gustatory thalamus or cortex eliminate avoidance of a taste cue when paired with either a drug of abuse or a rewarding sucrose solution, but not when paired with the aversive agent, LiCl. The present study used bilateral ibotenic acid lesions to evaluate the role of a neighboring thalamic structure, the trigeminal orosensory area (TOA), in avoidance of a gustatory cue when paired with sucrose (Experiment 1), morphine (Experiment 2), cocaine (Experiment 3), or LiCl (Experiment 4). The results show that the TOA lesion disrupts, but does not eliminate avoidance of a taste cue that predicts access to a preferred sucrose solution and leaves intact the development of a LiCl-induced conditioned taste aversion. The lesion does, however, eliminate the suppression of intake of a taste cue when paired with experimenter administered morphine or cocaine using our standard parameters. As such, this is the first manipulation found to dissociate avoidance of a taste cue when mediated by a sweet or by a drug of abuse.

Cocaine decreases saccharin preference without altering sweet taste sensitivity

“…This phenomenon has been interpreted a number of different ways. One hypothesis is that an anticipatory contrast effect develops where anticipation of the greater reward of cocaine decreases the normal reward value of saccharin (Grigson, 1997, Nyland et al , 2012). A competing hypothesis states that a form of taste avoidance learning occurs, where the drug-induced disruption of homeostasis causes a ‘taste shyness’ around saccharin when not self-administered (Hunt and Amit, 1987).…”

“…A short latency is generally associated with oral acceptability (Mantella and Youngentob, 2014, Nyland et al, 2012), while a long latency can be indicative of failure to learn the task, or of feared or unpleasant stimuli (Houpt et al, 2007). In our experiments, the mice are unaware of the precise stimulus presented.…”

“…For example, dopamine firing patterns in the nucleus accumbens are usually blunted after repeated access to sweet rewards, but not cocaine (Di Chiara et al , 2004, Rada et al , 2005). In addition, lesion studies have shown that taste circuits in the thalamus and projections from the parabrachial nucleus are essential for sweet- but not cocaine-elicited reward (Grigson et al, 2000, Norgren et al, 2006, Nyland et al, 2012). …”

Relative reward effects on operant behavior: Incentive contrast, induction and variety effects

“…This ‘Crespi Effect’ relied on a between group comparison with controls not experiencing an alteration of outcome value. Recent work on incentive contrast has found the effect to be more complicated than originally proposed (Binkley et al, 2014; Nyland et al, 2012; Ortega et al, 2011; King et al, 2002). Based on the complex but crucial nature of relative reward processing, it is vital that new paradigms are developed and explored to clarify interactions and overcome obstacles in understanding factors involved in incentive contrast as well as similar effects on behavior (Webber et al, 2011; Cromwell, 2010; Cromwell et al, 2005; Watanabe et al, 2001).…”

Striatal Activity and Reward Relativity: Neural Signals Encoding Dynamic Outcome Valuation

“…A contrast relative reward effect includes a significant difference in the predicted direction based on the contrast valence (greater shift for positive and reduced activity change for negative) between the sessions for a single-reward outcome experience. These specific functions could rely on striatal communication with other subcortical regions, such as the hippocampus, amygdala, and brainstem circuits (Liang et al, 2012; Nyland et al, 2012). Lesions to the hippocampus alter shifts in instrumental responses during negative contrast (Liao and Chuang, 2003).…”