Distinct regions of the periaqueductal gray are involved in the acquisition and expression of defensive responses

Abstract

In fear conditioning, a rat is placed in a distinct environment and delivered footshock. The response to the footshock itself is called an activity burst and includes running, jumping, and vocalization. The fear conditioned to the distinct environment by the footshock elicits complete immobility termed freezing. Lesions of the ventral periaqueductal gray (vPAG) strongly attenuate freezing. However, lesions of the dorsolateral periaqueductal gray (dlPAG) increase the amount of freezing seen to conditional fear cues acquired under conditions in which intact rats do not demonstrate much fear conditioning. To examine the necessity of these regions in the acquisition and expression of fear, we performed five experiments that examined the effects of electrolytic lesions of the dlPAG and the vPAG in learned and unlearned fear. In experiment 1, lesions of the vPAG strongly attenuated, whereas lesions of the dlPAG enhanced, unconditional freezing to a cat. In experiment 2, lesions of the dlPAG made before but not after training enhanced the amount of freezing shown to conditional fear cues acquired via immediate footshock delivery. In experiment 3, vPAG lesions made either before or after training with footshock decreased the level of freezing to conditional fear cues. Neither dlPAG lesions nor vPAG lesions affected footshock sensitivity (experiment 4) or consumption on a conditioned taste aversion test that does not elicit antipredator responses (experiment 5). On the basis of these results, it is proposed that activation of the dlPAG produces inhibition of the vPAG and forebrain structures involved with defense. In contrast, the vPAG seems to be necessary for postencounter freezing defensive behavior.

Fig. 1.

A representative sample of the location and extent of electrolytic lesions. Lesions of the dorsal PAG usually extended into the deep layers of the superior colliculus and the lateral PAG. Lesions of the ventral PAG included the lateral PAG and extended into the dorsal PAG.

Fig. 2.

Rats with lesions of the dlPAG or the vPAG in comparison with sham-lesioned rats showed enhanced or decreased levels of freezing, respectively, when presented with a cat.

Fig. 3.

Sham-lesioned rats receiving an immediate shock after placement in a chamber freeze comparably with rats that were not shocked. Rats receiving a pretraining dlPAG lesion (PRE-LESION) showed enhanced levels of freezing after training with immediate shock, whereas rats receiving a post-training dlPAG lesion (POST-LESION) did not. Pre- and post-training dlPAG lesions had no effect on rats that did not receive a shock.

Fig. 4.

Rats receiving a vPAG lesion either before (PRE-LESION) or after (POST-LESION) training with shock showed reduced levels of freezing compared with the group receiving a sham lesion at both times. Furthermore, the group receiving a post-training lesion showed greater attenuation of freezing than did the group receiving a pretraining lesion.

Fig. 5.

Rats with dlPAG, vPAG, or sham lesions did not differ in the shock intensity to which they flinched, jumped, or vocalized.

Fig. 6.

Rats with dlPAG, vPAG, or sham lesions did not differ in their consumption of a saccharin solution after toxicosis-induced taste aversion. W, Water;S, saccharin. Group SHAM-B received a backward pairing of saccharin and toxicosis and did not develop a taste aversion.