Taste uncoupled from nutrition fails to sustain the reinforcing properties of food

Abstract

Recent findings suggest the reward system encodes metabolic value independent of taste, provoking speculation that the hedonic value of taste could be derived from nutritional value as a secondary appetitive property. We therefore dissociated and compared the impact of nutrition and taste on appetitive behavior in several paradigms. Though taste alone induces preference and increased consumption, in the absence of nutritional value its reinforcing properties are greatly diminished and it does not, like sucrose, induce increased responding over time. In agreement with behavioral data, saccharin-evoked (but not sucrose-evoked) dopamine release is greatly attenuated following pre-exposure, suggesting that nutritional value is critical for dopamine-mediated reward and reinforcement. Further supporting the primacy of nutrition over taste, genetically increased dopaminergic tone enhances incentive associated with nutritional value with minimal impact on taste-based, hedonic incentive. Overall, we suggest that the sensory-hedonic incentive value associated with taste functions as a conditioned stimulus that requires nutritional value to sustainably organize appetitive behavior.

Figure 1

Effects of nutritional and hedonic value on consumption under conditions of free access. Throughout figures, colors code type of value: nutritional/metabolic only (blue), hedonic/taste only (red) or combined (purple). (A) Average daily consumption of tastant and water in wild-type mice provided a choice of either sucrose (filled squares) or sucralose (filled triangles) and water (open circles). (B/C) Average daily consumption of sucrose or sucralose (B, C respectively) and water (open symbols) in wild-type (filled squares) and trpm5 homozygous (filled triangles) mice. *** p < .001,** p < .01 * p < .05, vertical dashed lines indicate main effects. N = 12 (A/B), N = 6 (C/D).

Figure 2

Effect of quinine adulteration on consumption of sucrose or sucralose solution. Wild-type (A) consumption of tastant and water at various ratios of quinine and sweetener (dotted horizontal lines represent tastant consumption at baseline without quinine) and (B) preference for tastant over water (dotted horizontal line represents no preference mark). N = 8. Statistics in text.

Figure 3

Effect of elevated dopamine on consumption of tastants under conditions of free access. Average daily consumption of (A) sucrose or (B) sucralose for wild-type (filled squares), DATkd (open squares), trpm5 KO (filled triangles) and trpm5 KO:DATkd (open triangles). N = 6.

Figure 4

Conditioning induced by sucrose and sucralose in wild-type mice. Average consumption of (A) sucrose, (B) sucralose compared to water during conditioning sessions. (C) Relative consumption of sucrose or sucralose compared to water during each of three pairs of conditioning sessions. (D) Preference for bottle previously paired with either sucrose or sucralose compared to bottle previously paired to water. Dashed line marks no preference (ie., 50%). * p < .05, N = 6.

Figure 5

Effect of elevated dopamine on progressive ratio responding for hedonic and metabolic reward. (A) Average breakpoint across all sessions of PR7 for each reinforcer (blue ‘nutrition’ reflects sucrose with trpm5 KO mice) for mice with DATkd (light bars) and wild-type littermates (dark bars, either wild-type or trpm5 KO background). Dotted horizontal line represents median breakpoint. (B) Active lever presses for each day of the experiment for wild-type (filled symbols) and DATkd (open symbols) reinforced with sucrose (purple), calorie-free (combined sucralose and saccharin, red) or nutrition only (blue, sucrose tested with trpm5 KO background). In the left panel, the arrow represents where reinforcers were switched with the color continuing to indicate the reinforcer (ie., color will switch for same group/trace). *** p < .001, ** p < .01, * p < .05, N = 6.

Figure 6

Homecage progressive ratio concurrent choice effort and reward. (A) Effort: left panel, total active lever presses across days for wild-type (filled symbols) and DATkd (open symbols) reinforced with sucrose (purple), calorie-free (combined sucralose and saccharin, red) or nutrition only (blue, sucrose tested with trpm5 KO background). The arrow represents where reinforcers were switched with the color continuing to indicate the reinforcer (ie., color will switch for same group/trace). Right panel, average breakpoint for each reinforcer (sucrose, purple; calorie-free, red; sucrose with trpm5 KO, blue) split by DATkd (light bars) and wild-type or trpm5 KO (solid bars). (B) Consumption/rewards earned: same as in A. (C) Boxplots of preference for reinforcer as percentage of total consumption (reinforcer + chow) *** p < .001, ** p < .01, * p < .05. N = 6 (wild-type background) and = 5 (trpm5 background).

Figure 7

Phasic dopamine release evoked by saccharin pellets is attenuated relative to sucrose pellets. A. Experimental timeline. After 10 days training (starting with either sucrose or saccharin, counterbalanced) rats were surgically prepared for voltammetry recordings. After recovery, rats received two additional days training to habituate them to the recording headstage. During a single day of voltammetry recordings, rats received sucrose and saccharin pellets in blocks while phasic dopamine release was measured in nucleus accumbens core using fast-scan cyclic voltammetry. B. Left-hand panel, Behavioral data from training sessions showing that after several days of training rats retrieve and consume both types of pellet readily. Bars show mean ± SEM. Right-hand panel, Histological verification of electrode placements in nucleus accumbens core. Numbers are mm anterior to Bregma. Adapted from Paxinos and Watson (2008). C. Left-hand panel, Average heat map from all rats showing trial-by-trial analysis of pellet evoked dopamine with dopamine concentration coded by color, hot colors indicating high concentrations. Pellet evoked responses are strong during first block of sucrose pellets, ‘fade out’ during delivery of saccharin pellets, and return during the second block of sucrose pellets. Dashed lines indicate transitions between blocks. Right-hand panel, Single trial traces of dopamine concentration from a representative animal. D. Mean dopamine concentration traces for each block of trials (sucrose-saccharin-sucrose) with data normalized for each rat to peak dopamine concentration in block 1. Dotted lines show SEM. E. Peak pellet-evoked dopamine response as a function of trial number. Data are taken from maximum value in the 2 s after pellet delivery, indicated by white vertical lines in C. Mean ± SEM of all rats is shown for each trial and mean for each block is shown as horizontal line.