A neural systems analysis of the potentiation of feeding by conditioned stimuli

Abstract

Associative learning processes play many important roles in the control of food consumption. Although these processes can complement regulatory mechanisms in the control of eating by providing opportunities for the anticipation of upcoming needs, they may also contribute to inappropriate or pathological consumption patterns by overriding internal regulatory signals. In this article, we first review some of the ways in which associative learning can contribute to the control of feeding, and then describe a neural systems analysis of a simple animal model of the control of feeding by Pavlovian-conditioned stimuli (CSs). Food-sated rats increase their food consumption after presentation of CSs that were previously paired with food while the rats were food-deprived. This cue-potentiated feeding is independent of conditioned approach responses, and is at least somewhat specific to the foods associated with those CSs. A series of studies that used neuroanatomical tract tracing, immediate early gene expression, and neurotoxic disconnection lesion techniques implicated circuitry that includes the basolateral complex of the amygdala, the lateral hypothalamus, and the medial prefrontal cortex, but not the amygdala central nucleus, nucleus accumbens, or lateral orbitofrontal cortex, in cue-potentiated feeding. These studies also showed dissociations between cue-potentiated feeding and other learned motivational phenomena that are known to depend on function of amygdala systems. The data suggest that cue-potentiated feeding is uniquely mediated by cortical and amygdalar neurons that directly target the lateral hypothalamus, and thus gain access to hypothalamic neuropeptide and other systems involved in the promotion and suppression of eating.

Figure 1

Cue-potentiated feeding in rats with bilateral neurotoxic or sham lesions of (A) basolateral amgydala (BLA) or (B) central nucleus of the amygdala (CEA). The bars show the mean ± sem differences in the number of 45-mg food pellets consumed in tests with a previously reinforced conditioned stimulus or a previously nonreinforced stimulus. In separate tests, food pellets were presented in either the original food cups used in conditioning or in bowls placed elsewhere in the conditioning chambers.

Figure 2

Cue-potentiated feeding in rats with unilateral neurotoxic or sham lesions of the basolateral amgydala (BLA) and (A) the lateral hypothalamus (LH) or (B) the nucleus accumbens (ACB). In rats with contralateral lesions of BLA and LH or ACB, these regions were functionally disconnected from each other in both hemispheres, whereas in rats with ipsilateral lesions, communication was intact in one hemisphere. The bars show the mean ± sem differences in the number of 45-mg food pellets consumed in tests with a previously reinforced conditioned stimulus or a previously nonreinforced stimulus.

Figure 3

Cue-potentiated feeding in rats with bilateral neurotoxic or sham lesions of the medial prefrontal cortex (mPFC). Consumption of food pellets (in grams, mean ± sem) was measured in a context in which rats had previously been fed (paired) or not fed (unpaired) in the past.