Ontogeny of odor-LiCl vs. odor-shock learning: similar behaviors but divergent ages of functional amygdala emergence

Abstract

Both odor-preference and odor-aversion learning occur in perinatal pups before the maturation of brain structures that support this learning in adults. To characterize the development of odor learning, we compared three learning paradigms: (1) odor-LiCl (0.3M; 1% body weight, ip) and (2) odor-1.2-mA shock (hindlimb, 1 sec)--both of which consistently produce odor-aversion learning throughout life and (3) odor-0.5-mA shock, which produces an odor preference in early life but an odor avoidance as pups mature. Pups were trained at postnatal day (PN) 7-8, 12-13, or 23-24, using odor-LiCl and two odor-shock conditioning paradigms of odor-0.5-mA shock and odor-1.2-mA shock. Here we show that in the youngest pups (PN7-8), odor-preference learning was associated with activity in the anterior piriform (olfactory) cortex, while odor-aversion learning was associated with activity in the posterior piriform cortex. At PN12-13, when all conditioning paradigms produced an odor aversion, the odor-0.5-mA shock, odor-1.2-mA shock, and odor-LiCl all continued producing learning-associated changes in the posterior piriform cortex. However, only odor-0.5-mA shock induced learning-associated changes within the basolateral amygdala. At weaning (PN23-24), all learning paradigms produced learning-associated changes in the posterior piriform cortex and basolateral amygdala complex. These results suggest at least two basic principles of the development of the neurobiology of learning: (1) Learning that appears similar throughout development can be supported by neural systems showing very robust developmental changes, and (2) the emergence of amygdala function depends on the learning protocol and reinforcement condition being assessed.

Figure 1.

Gastrointestinal distress (diarrhea) in 0.5-mA shock-, 1.2-mA shock-, and LiCl-paired pups as a measure of malaise. *P < 0.05, significant difference from each group.

Figure 2.

Mean (± SEM) number of choices toward conditioned odor in the Y-maze test (total of five trails) for odor-0.5-mA shock, odor-1.2-mA shock, and odor-LiCl conditioning at PN7–8 (A), PN12–13 (B), and PN23–24 (C). *P < 0.05, significant difference from each control group.

Figure 3.

Pseudocolor 2-DG autoradiograph with the corresponding coronal brain section images from Paxinos and Watson (1986). The individual areas are outlined and labeled in the right images to indicate where optical densitomentric measurements were made in this study. aPC indicates anterior piriform cortex (A); pPC, posterior piriform cortex (B); and BLA, basolateral complex of amygdala (B). (Image reprinted with permission from Elsevier ©1986.)

Figure 4.

Mean (± SEM) relative anterior piriform cortex 2-DG uptake during odor-0.5-mA shock, odor-1.2-mA shock, and odor-LiCl conditioning at PN7–8 (A), PN12–13 (B), and PN23–24 (C). *P < 0.05, significant difference from each control group.

Figure 5.

Mean (± SEM) relative posterior piriform cortex 2-DG uptake during odor-0.5-mA shock, odor-1.2-mA shock, and odor-LiCl conditioning at PN7–8 (A), PN12–13 (B), and PN23–24 (C). *P < 0.05, significant difference from each control group.

Figure 6.

Mean (± SEM) relative amygdala basolateral complex 2-DG uptake during odor-0.5-mA shock, odor-1.2-mA shock, and odor-LiCl conditioning at PN7–8 (A), PN12–13 (B), and PN23–24 (C). *P < 0.05, significant difference from each control group.