Environmental modulation of alcohol intake in hamsters: effects of wheel running and constant light exposure

Abstract

Background: Alcohol abuse leads to marked disruptions of circadian rhythms, and these disturbances in themselves can increase the drive to drink. Circadian clock timing is regulated by light, as well as by nonphotic influences such as food, social interactions, and wheel running. We previously reported that alcohol markedly disrupts photic and nonphotic modes of circadian rhythm regulation in Syrian hamsters. As an extension of this work, we characterize the hedonic interrelationship between wheel running and ethanol (EtOH) intake and the effects of environmental circadian disruption (long-term exposure to constant light [LL]) on the drive to drink.

Methods: First, we tested the effect of wheel running on chronic free-choice consumption of a 20% (v/v) EtOH solution and water. Second, the effect of this alcohol drinking on wheel running in alcohol-naive animals was investigated. Third, we assessed the influence of LL, known to suppress locomotor activity and cause circadian rhythm disruption, on EtOH consumption and wheel-running behavior.

Results: Inhibitory effects of wheel running on EtOH intake and vice versa were observed. Exposure to LL, while not affecting EtOH intake, induced rhythm splitting in 75% of the animals. Notably, the splitting phenotype was associated with lower levels of EtOH consumption and preference prior to, and throughout, the period of LL exposure.

Conclusions: These results are evidence that exercise may offer an efficacious clinical approach to reducing EtOH intake. Also, predisposition for light-induced (or other) forms of circadian disruption may modulate the drive to drink.

Figure 1

Wheel running suppresses EtOH consumption. Top graph: mean daily ethanol consumption for all animals (dashed line; these animals were considered statistically as a single group, as they were not randomly separated into running and non-running groups until the start of Phase II), runners (solid line), and non-runners (dotted line). Phase I: ethanol acclimation period (wheels locked). Phase II (shaded): wheels unlocked for experimental group and locked for controls. Phase III: all wheels locked. Bottom graph: ethanol consumption and preference for runners and non-runners averaged over each phase. Bars represent means±SEM. Among all groups and phases, bars with different letters are significantly different (p<0.05).

Figure 2

EtOH consumption suppresses wheel running. Top graph: daily distance run by animals given free-choice between 20% ethanol and water (solid line) or water only (dotted line). Shaded area represents wheel acclimation period; EtOH introduction occurred at the beginning of the non-shaded region. Bottom graph: distance run by drinkers (EtOH) and non-drinkers (water) during the initial 3 wks of EtOH drinking. Bars represent means±SEM. Bars with different letters are significantly different (p<0.05).

Figure 3

Representative double-plotted actograms of wheel-running activity of free-choice 20% EtOH drinking hamsters showing a free-running non-split rhythm (top) and split rhythm (bottom). The shaded area designates the initial LD photocycle; the unshaded area designates LL.

Figure 4

Suppression of general daily locomotor activity (expressed as mean daily bout number × mean daily bout duration) by exposure to LL. Locomotor activity is maximally suppressed compared to LD levels during the initial 3 days of LL treatment assessed in all hamsters. This activity was also suppressed in hamsters of the rhythm splitting phenotype immediately prior to and during splitting. Bars represent means±SEM. Bars with different letters are significantly different (p<0.05).

Figure 5

Wheel-running distance (top panel), free-choice 20% EtOH consumption (middle panel) and EtOH preference (bottom panel) for hamsters under LL exhibiting non-split and split rhythms (middle and right side, respectively) and averaged for all hamsters (Group; left side). Gray bars represent the averages measured under the initial LD photocycle. White bars represent the first and last 5 days of LL. Bars represent means±SEM. For each parameter, bars with different letters are significantly different (p<0.05).

Figure 6

Mean daily EtOH consumption (top panel) and wheel-running distance (bottom panel) for splitting (solid line) and non-splitting (dotted line) hamsters on free-choice 20% EtOH under LL.