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Distinct Regions of the Periaqueductal Gray Are Involved in the Acquisition and Expression of Defensive Responses

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Distinct Regions of the Periaqueductal Gray Are Involved in the Acquisition and Expression of Defensive Responses The Journal of Neuroscience, May 1, 1998, 18(9):3426–3432 Distinct Regions of the Periaqueductal Gray Are Involved in the Acquisition and Expression of Defensive Responses Beatrice M. De Oca, Joseph P. DeCola, Stephen Maren, and Michael S. Fanselow Department of Psychology, University of California, Los Angeles, Los Angeles, California 90024-1563 In fear conditioning, a rat is placed in a distinct environment and hanced, unconditional freezing to a cat. In experiment 2, lesions delivered footshock. The response to the footshock itself is of the dlPAG made before but not after training enhanced the called an activity burst and includes running, jumping, and amount of freezing shown to conditional fear cues acquired via vocalization. The fear conditioned to the distinct environment immediate footshock delivery. In experiment 3, vPAG lesions by the footshock elicits complete immobility termed freezing. made either before or after training with footshock decreased Lesions of the ventral periaqueductal gray (vPAG) strongly at- the level of freezing to conditional fear cues. Neither dlPAG tenuate freezing. However, lesions of the dorsolateral periaq- lesions nor vPAG lesions affected footshock sensitivity (exper- ueductal gray (dlPAG) increase the amount of freezing seen to iment 4) or consumption on a conditioned taste aversion test conditional fear cues acquired under conditions in which intact that does not elicit antipredator responses (experiment 5). On rats do not demonstrate much fear conditioning. To examine the basis of these results, it is proposed that activation of the the necessity of these regions in the acquisition and expression dlPAG produces inhibition of the vPAG and forebrain structures of fear, we performed five experiments that examined the ef- involved with defense. In contrast, the vPAG seems to be fects of electrolytic lesions of the dlPAG and the vPAG in necessary for postencounter freezing defensive behavior. learned and unlearned fear. In experiment 1, lesions of the Key words: periaqueductal gray; midbrain; freezing; fear con- vPAG strongly attenuated, whereas lesions of the dlPAG en- ditioning; unconditional fear; defense When rats are placed in a distinct environment and shocked, two ation of startle compared with intermediate shock intensities behaviors can be observed. Circastrike responding involves run- (Davis and Astrachan, 1978). Because potentiated startle levels ning, jumping, and vocalization and is elicited directly by foot- increased during the course of extinction of conditional fear, an shock. The other response is freezing. Freezing is complete inverse relationship between fear and potentiated startle is sug- immobility except for that required for breathing. Freezing is not gested. Lesions of the dlPAG made after fear conditioning blocked elicited directly by the shock but by the fear to the chamber the attenuation of potentiated startle seen with high shock inten- conditioned by the footshock (Blanchard and Blanchard, 1969; sities, allowing for the levels of fear potentiation that occur with Bolles and Collier, 1976; Fanselow, 1980). Electrolytic lesions of high shock intensities and with intermediate shock intensities to be the dorsolateral periaqueductal gray (dlPAG) result in enhanced similar. In addition, stimulation of the dlPAG with nontoxic doses freezing to contextual cues paired with footshock under circum- of kainic acid attenuated the potentiated startle elicited in the stances in which intact rats freeze little (Fanselow et al., 1995). presence of cues fear-conditioned with moderate shock (Walker Because dlPAG lesions facilitate conditional fear, three roles and Davis, 1997). Thus, stimulation of the dlPAG during fear- for the dlPAG are possible: (1) the dlPAG may inhibit the amyg- potentiated startle to a cue trained with moderate levels of shock dala or other forebrain structures involved in processing fear- produced behavior typical of that seen when high shock intensities provoking stimuli; (2) the dlPAG may interfere with the perfor- were used. The authors concluded that the dlPAG may inhibit mance of fear-motivated behavior; and (3) the dlPAG may amygdaloid terminals that synapse onto the fear-potentiated startle produce a brief analgesia elicited by shocks that in turn interferes circuit at the level of nucleus reticularis pontis caudalis. with the acquisition of fear. An instance of shock interfering with acquisition instead of One technique in which support for the second option has been performance occurs with massed and immediate shock delivery. obtained is fear-potentiated startle. In fear-potentiated startle, the When shocks are delivered close together in time (Fanselow and acoustic startle response is enhanced by cues signaling footshock. Tighe, 1988) or immediately after the placement of a rat in the There is a nonmonotonic function between the shock intensity chamber (Blanchard and Blanchard, 1971), no conditional fear is used during fear conditioning and the potentiated startle. When a acquired. One reason may be that shock interferes with the pro- conditional stimulus (CS) is trained with high shock intensities, there is a diminution of the magnitude of the subsequent potenti- cessing of the context by the animal (Fanselow, 1986), thus com- promising the context–shock association. That dlPAG lesions at- Received May 27, 1997; revised Feb. 9, 1998; accepted Feb. 13, 1998. tenuate these effects (Fanselow et al., 1995) suggests that activation This work was supported by National Institute of Mental Health Grant MH 39786 of the dlPAG in intact rats may interfere with or inhibit other to M.S.F. Correspondence should be addressed to Dr. Beatrice M. De Oca, Department of structures like the amygdala that are involved in the acquisition of Social Sciences, Western New Mexico University, Box 680, 1000 West College conditional fear. However, when the shocks are widely spaced or Avenue, Silver City, NM 88062. delivered after contextual cues are processed, conditioning can still Dr. Maren’s present address: Department of Psychology, University of Michigan, 525 East University Avenue, Ann Arbor, MI 48109-1109. occur, suggesting a brief rather than a sustained inhibition by the Copyright © 1998 Society for Neuroscience 0270-6474/98/183426-07$05.00/0 dlPAG. If the lesion indeed prevents the inhibition of other struc- De Oca et al. • PAG and Defense J. Neurosci., May 1, 1998, 18(9):3426–3432 3427 tures during conditioning, then only lesions made before testing but sioned area is necessary for the production of defensive behavior. Elec- not after should eliminate the effect of massed or immediate shock trolytic lesions will be used instead of excitotoxic lesions because of the risks associated with infusion of neurotoxins in close proximity to the delivery. This hypothesis will be tested in experiment 2. cerebral aqueduct. Furthermore, all previous parametric work with these The model proposed by Fanselow (1991) suggests that the procedures has used electrolytic lesions. The continued use of electro- ventral periaqueductal gray (vPAG) is exclusively involved in the lytic lesions will allow direct comparison between the behavioral results expression of fear, whereas forebrain structures such as the amyg- with these experiments and other experiments done in the laboratory dala that communicate with the PAG are involved in acquisition. without confounding lesion type. Behavioral apparatus. The testing apparatus of the first experiment In contrast to this view, there are data suggesting a role for the consisted of a large 60 3 58.5 3 61 cm plywood container with a clear vPAG in the acquisition of conditional fear. Administration of acrylic ceiling and a clear acrylic glass door through which all behavior acoustic startle stimuli produces both startle and freezing. Pre- was observed and video recorded. Inside the enclosure, proximal to the sumably, this freezing occurs because the apparatus serves as a door in one corner, was an empty, clear glass aquarium (24.5 3 25.5 3 CS and the startle cues serve as an unconditional stimulus (US). 25.5 cm) with a hinged door on the top; the rat was placed in this enclosure for the test. The ceiling of the aquarium had a small protruding Conditional fear to apparatus cues and habituation of acoustic spout, allowing for air to enter and exit the aquarium. On sessions in startle are negatively correlated (Leaton and Borszcz, 1985). which the cat was used, it was placed inside the larger enclosure such that Procedures that weaken fear conditioning like latent inhibition or the rat and cat could see and smell each other, but contact between the extinction of the CS facilitate habituation of startle responses. two was impossible. The cat was an adult domestic cat. Lesions of the vPAG also facilitated habituation of acoustic startle The apparatus used in all other experiments consisted of an observation chamber (21 3 28 3 20.5 cm) made of stainless steel walls and a clear (Borszcz et al., 1989). According to the authors, fear conditioned acrylic ceiling and door. The chamber contained a stainless steel rod floor, to the apparatus serves to sensitize responses to the acoustic with 18 0.4 mm rods placed 1.0 cm apart, center to center. Before each use, stimuli, and lesions of the vPAG attenuated this conditional fear. the chambers were cleaned with a 5% ammonium hydroxide solution, and However, when behavioral and autonomic measures of condi- a light coating of this ammonium hydroxide solution was placed in the litter pans underneath the grid floor. The chamber lay within a sound- tional fear are assessed, only the behavioral response freezing was attenuating chest that was free of its door to facilitate observation by the attenuated by lesions of the PAG (LeDoux et al., 1988). Another experimenter. Scrambled electric shock originated from a custom 450 V AC goal of the present research is to see whether the vPAG plays a shock source wired through a mechanical scrambler (Lafayette Instruments critical role exclusively during training. Co.). This equipment was in an isolated room of the laboratory that was lit The present series of experiments examines the behavior of by two fluorescent ceiling fixtures.
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