Physiological mechanisms for food-hoarding motivation in animals

Abstract

The study of ingestive behaviour has an extensive history, starting as early as 1918 when Wallace Craig, an animal behaviourist, coined the terms 'appetitive' and 'consummatory' for the two-part sequence of eating, drinking and sexual behaviours. Since then, most ingestive behaviour research has focused on the neuroendocrine control of food ingestion (consummatory behaviour). The quantity of food eaten, however, is also influenced by the drive both to acquire and to store food (appetitive behaviour). For example, hamster species have a natural proclivity to hoard food and preferentially alter appetitive ingestive behaviours in response to environmental changes and/or metabolic hormones and neuropeptides, whereas other species would instead primarily increase their food intake. Therefore, with the strong appetitive component to their ingestive behaviour that is relatively separate from their consummatory behaviour, they seem an ideal model for elucidating the neuroendocrine mechanisms underlying the control of food hoarding and foraging. This review focuses on the appetitive side of ingestive behaviour, in particular food hoarding, attempting to integrate what is known about the neuroendocrine mechanisms regulating this relatively poorly studied behaviour. An hypothesis is formed stating that the direction of 'energy flux' is a unifying factor for the control of food hoarding.

Figure 1.

(a,b) Effects of (a) ghrelin treatment on plasma active ghrelin concentrations at time points from 0 to 48 h post-injection and (b) 0–48 h of food deprivation on plasma active ghrelin concentrations at 12-h time intervals, p < 0.05 for different letters. (c–e) Mean + s.e.m. food hoarding (pellets hoarded) as a percentage of the saline-injected controls for the effects of peripheral ghrelin treatment. (c) Hamsters with no foraging requirement and a blocked running wheel (blocked wheel), (d) hamsters with no foraging requirement but a freely moving wheel (free wheel group), and (e) hamsters with a foraging requirement of 10 revolutions per food pellet (10 revolutions per pellet group), *p < 0.05 compared with saline injection. Adapted from Keen-Rhinehart & Bartness (2005). Copyright © American Physiological Society.

Figure 2.

(a,b) Effects of (a) leptin treatment on plasma leptin concentrations at time points from 0 to 24 h post-injection and (b) 48 h of food deprivation on plasma leptin concentrations. Black bars, leptin (0); dark grey bars, leptin (10 µg); light grey bars, leptin (40 µg); white bars, leptin (80 µg), *p < 0.05 compared with ad libitum baseline concentrations. (c–e) Effects of peripheral leptin treatment on food hoarding in (c) hamsters with no foraging requirement and a blocked running wheel (blocked wheel), (d) hamsters with no foraging requirement but a freely moving wheel (free wheel group), and (e) hamsters with a foraging requirement of 10 revolutions per food pellet (10 revolutions per pellet group), *p < 0.05 compared with saline injection. Black bars, leptin (0); grey bars, leptin (10 µg); striped bars, leptin (40 µg); white bars, leptin (80 µg). 48 h FD, 48 h of food deprivation. Adapted from Keen-Rhinehart & Bartness (2008). Copyright © American Physiological Society.

Figure 3.

Ability of central leptin treatment to counteract the effects of food deprivation on food hoarding in (a) hamsters with no foraging requirement and a blocked running wheel (blocked wheel), (b) hamsters with no foraging requirement but a freely moving wheel (free wheel group), and (c) hamsters with a foraging requirement of 10 revolutions per food pellet (10 revolutions per pellet group), *p < 0.05 compared with saline injection. Black bar, leptin (0); grey bar, leptin (1.25 µg); striped bar, leptin (2.5 µg); white bar, leptin (5 µg). Adapted from Keen-Rhinehart & Bartness (2008). Copyright © American Physiological Society.

Figure 4.

Ability of an NPY Y1R antagonist (1229U91) to counteract the effects of (a–c) ghrelin treatment (Black bar, saline + ghrelin; grey bar, saline + 1229U91; striped bar, ghrelin + 1229U91)) and (d–f) food deprivation (FD) on food hoarding (black bar, FD; grey bar, FD + 1229U91). Effects of central 1229U91 treatment on food hoarding after peripheral ghrelin treatment in (a) hamsters with no foraging requirement and a blocked running wheel (blocked wheel), (b) hamsters with no foraging requirement but a freely moving wheel (free wheel group), and (c) hamsters with a foraging requirement of 10 revolutions per food pellet (10 revolutions per pellet group). Effects of central 1229U91 treatment on food hoarding after 48 h of food deprivation in (d) hamsters with no foraging requirement and a blocked running wheel (blocked wheel), (e) hamsters with no foraging requirement but a freely moving wheel (free wheel group), and (f) hamsters with a foraging requirement of 10 revolutions per food pellet (10 revolutions per pellet). *p < 0.05 compared with saline injection. Adapted from Keen-Rhinehart & Bartness (2007b). Copyright © American Physiological Society.

Figure 5.

Ability of a melanocortin-3/4R agonist (MTII) to counteract the effects of (a–c) peripheral ghrelin treatment (black bar, saline; grey bar, saline + ghrelin; striped bar, MTII + saline; white bar, MTII + ghrelin) and (d–f) food deprivation (FD) on food hoarding (black bar, FD; grey bar, FD + MTII). Effects of central MTII treatment on food hoarding after peripheral ghrelin treatment in (a) hamsters with no foraging requirement and a blocked running wheel (blocked wheel), (b) hamsters with no foraging requirement but a freely moving wheel (free wheel group), and (c) hamsters with a foraging requirement of 10 revolutions per food pellet (10 revolutions per pellet group). Effects of central MTII treatment on food hoarding after 48 h of food deprivation in (d) hamsters with no foraging requirement and a blocked running wheel (blocked wheel), (e) hamsters with no foraging requirement but a freely moving wheel (free wheel group), and (f) hamsters with a foraging requirement of 10 revolutions per food pellet (10 revolutions per pellet group). *p < 0.05 compared with saline injection. Adapted from Keen-Rhinehart & Bartness (2007a). Copyright © Elsevier.