Exploring Adaptations to Famine: Rats Selectively Bred for Differential Intake of Saccharin Differ on Deprivation-Induced Hyperactivity and Emotionality

Abstract

In many mammals, including humans and rats, acute starvation increases locomotor activity. This seemingly paradoxical and potentially lethal behavior pattern may reflect an evolved, multisystem response to sudden threats to metabolic homeostasis. The present study provides a novel test of this idea. Occidental High-(HiS) and Low-(LoS) Saccharin-Consuming rats differ on the taste phenotype and also on some affective measures, on which LoS rats score higher. Wheel running was measured in HiS and LoS rats with food available freely versus for 1 hr daily. As predicted, restricted feeding stimulated significantly more running among LoS rats. Two independent tests of emotionality (acoustic startle, stress-induced analgesia) also distinguished the lines. The confluence of taste, emotion, and reactivity to starvation conditions in species as distantly related as rats and humans points to integrated biobehavioral systems that warrant further exploration.The venerable concepts of metabolic homeostasis and "set point" can be challenged in interesting ways. An example is the excessive exercise that often accompanies reduced food intake in humans and other animals (Epling & Pierce, 1996;Pierce & Epling, 1997; Vincent & Parϑ, 1976). For humans, this pattern is associated with the clinical diagnoses of anorexia and bulimia nervosa (American Psychiatric Association, DSM IV, 1994). Because activity increases in starvation conditions -when conserving energy seems more logical -deprivation-induced hyperactivity (DIH) is sometimes termed "paradoxical" or, in humans, "irrational" and "selfdestructive." Its occurrence in intact, healthy rats, however, implicates phylogenetically old systems, perhaps constituting co-evolved adaptations to famine: Although relocating during a severe food shortage would consume resources and not guarantee survival, it may have, on balance, conferred a selective advantage over remaining in a depleted food patch (Pierce & Epling, 1996).

Temporal Organization of Eating in Low- and High- Saccharin-Consuming Rats

“…More importantly, line differences in the parameters were statistically the same in females and in males. The line difference also has been essentially the same in females and in males in other studies with both sexes: Differences between LoS and HiS rats in open-field emergence (Dess & Minor, 1996), acoustic startle (Dess et al, 2000), and intake of flavored solutions and ethanol Dess, 2000) were not sex specific. While the magnitude of the line difference sometimes differed between sexes, the direction of the -326 -difference and its sensitivity to parametric manipulation were comparable in females and in males.…”

“…This prediction is counterintuitive in the sense that one might expect rats who are more reactive to metabolic emergency to eat faster, not slower. It is, however, reminiscent of prior observations that LoS rats eat less than do HiS rats in response to hypoglycemia produced by fast-acting insulin or 2-deoxy-D-glucose (VanderWeele et al, 2002) and respond to food deprivation with a staggering increase in energy expenditure by running (Dess et al, 2000). Also, in the delaydiscounting procedure, hungry LoS rats are more willing than HiS rats to tolerate a delay to earn a larger food reward (Perry, Nelson, Anderson, Morgan, & Carroll, 2007); the lines did not differ when cocaine was the reward, implicating energy regulation rather than generic incentive value in the effect.…”

“…Phenotypic correlates also include behaviors bearing no obvious relationship to appetitive motivation. Relative to HiS rats, LoS rats score higher on several measures of emotional reactivity including defecation in a novel open field (Dess & Minor, 1996), acoustic startle amplitude (Dess et al, 2000), ethanol withdrawal (Dess, O'Neill, & Chapman, 2005), and stress-induced hypoalgesia (Dess et al, 2000).…”

“…Steady state cyclic ratio performance of LoS and HiS rats was examined in Experiment 1. LoS rats are more reactive to metabolic challenges including -323 -hypoglycemia (VanderWeele et al, 2002) and restricted access to food (Dess et al, 2000). Thus, the chronic food deprivation required for stable performance on this schedule should constitute a greater stressor for LoS rats than for HiS rats.…”

“…In an early one (Dess & Minor 1996), LoS rats showed greater suppression of homecage food intake by a stressor than did HiS rats, an effect consistent with a regulatory shift toward utilization of stored nutrients. Later, we reported in this journal (Dess et al, 2000) that deprivation-induced hyperactivity (DIH) is greater among LoS rats. When fed one hour per day for two days, LoS rats run more than twice as much in a wheel as HiS rats.…”