Dissociable effects of disconnecting amygdala central nucleus from the ventral tegmental area or substantia nigra on learned orienting and incentive motivation - PubMed (original) (raw)

Dissociable effects of disconnecting amygdala central nucleus from the ventral tegmental area or substantia nigra on learned orienting and incentive motivation

Heather El-Amamy et al. Eur J Neurosci. 2007 Mar.

Abstract

Recent evidence suggests that the amygdala central nucleus (CeA) and midbrain-striatal dopamine systems are critically involved in the alteration of attentional and emotional processing of initially neutral stimuli by associative learning. In rats, the acquisition of learned orienting responses (ORs) to visual cues paired with food is impaired by lesions of the CeA, and by lesions that disconnect CeA from the dorsolateral striatum (DLS), a region traditionally implicated in elevated responsiveness to sensory stimuli. Similarly, the acquisition of emotional significance to cues paired with food also depends on the function of CeA and of the ventral striatal nucleus accumbens (ACB), a region often considered crucial to acquired reward and motivation. For example, the ability of a cue previously paired with food to increase the rate of food-reinforced instrumental responding (Pavlovian-instrumental transfer, PIT) is eliminated by lesions of the CeA or the accumbens core. In this experiment, we found that lesions that functionally disconnected CeA from the substantia nigra pars compacta (SNc) impaired the acquisition of conditioned orienting to auditory cues paired with food, but had no effect on their ability to enhance instrumental responding, relative to the effects of unilateral lesions of that region. By contrast, lesions that disconnected CeA from the ventral tegmental area (VTA) had no effect on the acquisition of conditioned orienting, but facilitated Pavlovian-instrumental transfer relative to unilateral midbrain lesions, rescuing that function to sham-lesion control levels. Otherwise, unilateral lesions of either midbrain region impaired transfer. Implications of these results for circuit models of amygdalo-striatal interactions in associative learning are discussed.

PubMed Disclaimer

Figures

Figure 1

Sample lesions. The top two panels show Nissl-stained coronal sections of the amygdala in the lesioned (panel A) and unlesioned (panel B) hemispheres. Panel A shows substantial neuron loss and gliosis in amygdala central nucleus (CeA), with little loss in the adjoining basolateral amygdala (BLA). Panels C and H show sections stained for tyrosine hydroxylase in brains with lesions of the ventral tegmental area (VTA; panel C) or substantia nigra pars compacta (SNc; panel H). Panels D-G show higher magnifications of the section shown in panel C and panels I-L show higher magnifications of the section shown in panel H. Panels D, F, I, and J show the lesioned side and panels E, G, J, and L show the unlesioned side. Panels D, E, I, and J show VTA and Panels F, G, K, and L show SNc.

Figure 2

Orienting responses (panels A and B) and food cup (panels C and D) responses to the reinforced auditory conditioned stimulus (CS+; panels A and C) and the nonreinforced stimulus (CS−; panels B and D) in the first three experimental phases. Rats first received nonreinforced presentations of noise and tone stimuli in the pretest session, then pairings of one of those stimuli with sucrose during 3 nondiscriminative conditioning sessions (c1-c3), and finally continued pairings of that stimulus with sucrose, along with nonreinforced presentations of the other stimulus, in 10 discriminative conditioning sessions (d1-d10). Prior to training, some rats received lesions that disconnected amygdala central nucleus (CeA) from either the substantia nigra pars compacta (Group SNc-contra) or the ventral tegmental area (Group VTA-contra). Two unilateral lesion control groups received lesions of SNc or VTA in one hemisphere and either neurotoxic or sham lesions of CeA in the same hemisphere (Groups SNc-uni and VTA-uni, respectively). Lesion control rats (Group CTL) received sham lesions of both CeA and either SNc or VTA. Relative to all other groups, disconnection of CeA and SNc (Group SNc-Contra) significantly impaired the acquisition of conditioned ORs (A) but not food cup responses (C), and had no effect on unconditioned ORs (A). There were no significant between-group differences in the loss of generalized responding to the nonreinforced cue (CS−) over the course of discrimination training.

Figure 3

Results of the test of Pavlovian-instrumental transfer. Panel A shows the elevation in lever press rate over baseline produced by the auditory conditioned stimulus that previously was paired with sucrose (CS+). Panel B shows the elevations produced by the auditory stimulus that was previously nonreinforced (CS−). Panel C shows the baseline rates of lever pressing from which the elevation scores in panels A and B were derived.

References

1. Acheson AL, Zigmond MJ, Stricker EM. Compensatory increase in tyrosine hydroxylase activity in rat brain after intraventricular injections of 6-hydroxydopamine. Science. 1980;207:537–540. - PubMed
1. Ahn S, Phillips AG. Dopaminergic correlates of sensory-specific satiety in the medial prefrontal cortex and nucleus accumbens of the rat. J. Neurosci. 1999;19:1–6. - PMC - PubMed
1. Ahn S, Phillips AG. Modulation by central and basolateral amygdalar nuclei of dopaminergic correlates of feeding to satiety in the rat nucleus accumbens and medial prefrontal cortex. J. Neurosci. 2002;22:10958–10965. - PMC - PubMed
1. Amaral DG, Price JL, Pitkänen A, Carmichael ST. Anatomical organization of the primate amygdaloid complex. In: Aggleton JP, editor. The Amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction. Wiley-Liss; New York: 1992. pp. 1–66.
1. Berridge KC, Robinson TE. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res. Rev. 1998;28:309–369. - PubMed

Dissociable effects of disconnecting amygdala central nucleus from the ventral tegmental area or substantia nigra on learned orienting and incentive motivation - PubMed (original) (raw)