Sheep use preingestive cues as indicators of postingestive consequences to improve food learning

Previous work has shown that herbivores successfully learn to associate food sensory characteristics with postingestive consequences when the conditioning procedure is simple, whereas this ability breaks down when the learning task is made more complex. We hypothesized that sensory characteristics could act as indicators of postingestive consequences and that the presence of preingestive cues would improve the food learning of sheep in situations varying in complexity. Sixteen sheep were subjected to a first conditioning phase to associate 2 flavors added to alfalfa hay with either a positive or a negative consequence, induced by intraruminal administration of starch (330 mg/g of DMI) or LiCl (5 mg/g of DMI). Sheep progressively decreased their choice of the flavored hay associated with the negative consequence (P < 0.05). This procedure provided sheep with experience with postingestive consequences associated with the different flavors. In a second conditioning phase, the experienced sheep and 16 naïve sheep were divided into groups of 8 and subjected to either a simple or a complex conditioning procedure [i.e., the 2 flavors were offered on separate days (simple conditioning) or simultaneously within a day (complex conditioning)]. The 2 flavors applied to grass hay were associated with either positive (starch, 330 mg/g of DMI) or negative (LiCl, 10 mg/g of DMI) consequences. As hypothesized, sheep in the simple conditioning group expressed a greater aversion to the flavored hay associated with the negative consequence than did those in the complex conditioning group (0.303 +/- 0.035 vs. 0.474 +/- 0.035 respectively; P < 0.01). Experienced sheep rejected the flavor associated with the negative consequence more strongly than did naïve sheep, regardless of the conditioning procedure (0.304 +/- 0.029 vs. 0.470 +/- 0.041 respectively; P < 0.05). The initial increased preference for aniseed (0.80 +/- 0.04), however, greatly influenced food learning because sheep negatively conditioned on this flavor expressed less avoidance than those negatively conditioned on orange (0.53 +/- 0.04 vs. 0.25 +/- 0.03 respectively; P < 0.01). In conclusion, the simultaneous scenario was actually perceived as complex by all sheep, and experienced sheep were more efficient in food learning than naïve sheep in both the simple and complex learning contexts. The sheep were thus able to generalize the association between sensory cues and postingestive consequences, especially in a complex environment, and then to use these sensory cues as indicators of postingestive consequences.