Evidence of Pavlovian conditioned fear following electrical stimulation of the periaqueductal grey in the rat

Scala, Georges Di; Mana, Michael J.; Jacobs, W. Jake; Phillips, A. G.

doi:10.1016/0031-9384(87)90185-5

Cited by 79 publications

(50 citation statements)

References 39 publications

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“…This effect may not be attributed to reflexive motor responses, since it was not observed when the neutral stimulus was presented alone, as demonstrated in a previous study from this laboratory (10). The pattern of results obtained in the present experiments with light as a warning stimulus parallels those which use a conditioned stimulus paired with stimulation of the dorsal periaqueductal gray (19,20). It is likely that the inferior colliculus may be responsible for the elaboration of aversion and fear-like responses, together with other structures of the brain aversion system, such as dorsal periaqueductal gray matter and amygdala.…”

Section: Discussionsupporting

confidence: 85%

“…Evidence showing that the steps of sensory processing are modulated during learning procedures (24,25) supports this possibility. Interestingly, pairing tone with stimulation of the midbrain tectum, in which several sites of stimulation were located in the superior colliculus, a relay for visual information, produces a strong conditioning compared to a weak one when light was used as the conditioned stimulus (19).…”

Section: Discussionmentioning

confidence: 99%

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Signaled two-way avoidance learning using electrical stimulation of the inferior colliculus as negative reinforcement: effects of visual and auditory cues as warning stimuli

Troncoso

Cirilo-Júnior

Sandner

et al. 1998

Braz J Med Biol Res

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The inferior colliculus is a primary relay for the processing of auditory information in the brainstem. The inferior colliculus is also part of the so-called brain aversion system as animals learn to switch off the electrical stimulation of this structure. The purpose of the present study was to determine whether associative learning occurs between aversion induced by electrical stimulation of the inferior colliculus and visual and auditory warning stimuli. Rats implanted with electrodes into the central nucleus of the inferior colliculus were placed inside an open-field and thresholds for the escape response to electrical stimulation of the inferior colliculus were determined. The rats were then placed inside a shuttle-box and submitted to a two-way avoidance paradigm. Electrical stimulation of the inferior colliculus at the escape threshold (98.12 ± 6.15 (A, peak-to-peak) was used as negative reinforcement and light or tone as the warning stimulus. Each session consisted of 50 trials and was divided into two segments of 25 trials in order to determine the learning rate of the animals during the sessions. The rats learned to avoid the inferior colliculus stimulation when light was used as the warning stimulus (13.25 ± 0.60 s and 8.63 ± 0.93 s for latencies and 12.5 ± 2.04 and 19.62 ± 1.65 for frequencies in the first and second halves of the sessions, respectively, P<0.01 in both cases). No significant changes in latencies (14.75 ± 1.63 and 12.75 ± 1.44 s) or frequencies of responses (8.75 ± 1.20 and 11.25 ± 1.13) were seen when tone was used as the warning stimulus (P>0.05 in both cases). Taken together, the present results suggest that rats learn to avoid the inferior colliculus stimulation when light is used as the warning stimulus. However, this learning process does not occur when the neutral stimulus used is an acoustic one. Electrical stimulation of the inferior colliculus may disturb the signal transmission of the stimulus to be conditioned from the inferior colliculus to higher brain structures such as amygdala.

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Section: Discussionsupporting

confidence: 85%

Section: Discussionmentioning

confidence: 99%

Signaled two-way avoidance learning using electrical stimulation of the inferior colliculus as negative reinforcement: effects of visual and auditory cues as warning stimuli

Troncoso

Cirilo-Júnior

Sandner

et al. 1998

Braz J Med Biol Res

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“…This finding does not discard that associative learning may still be formed using stimulation of the aversive substrates of the dPAG as already clearly shown by other investigators (DiScala et al 1987). However, the parameters used to produce associative learning using dPAG stimulation need to be stronger that the ones used in the present experiment.…”

Section: Vianna Et Alsupporting

confidence: 72%

Lesion of the Ventral Periaqueductal Gray Reduces Conditioned Fear but Does Not Change Freezing Induced by Stimulation of the Dorsal Periaqueductal Gray

Vianna¹,

Graeff²,

Landeira-Fernández³

et al. 2001

Learn. Mem.

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Previously-reported evidence showed that freezing to a context previously associated with footshock is impaired by lesion of the ventral periaqueductal gray (vPAG). It has also been shown that stepwise increase in the intensity of the electrical stimulation of the dorsal periaqueductal gray (dPAG) produces alertness, then freezing, and finally escape. These aversive responses are mimicked by microinjections of GABA receptor antagonists, such as bicuculline, or blockers of the glutamic acid decarboxylase (GAD), such as semicarbazide, into the dPAG. In this work, we examined whether the expression of these defensive responses could be the result of activation of ventral portion of the periaqueductal gray. Sham- or vPAG electrolytic–lesioned rats were implanted with an electrode in the dPAG for the determination of the thresholds of freezing and escape responses. The vPAG electrolytic lesions were behaviorally verified through a context-conditioned fear paradigm. Results indicated that lesion of the vPAG disrupted conditioned freezing response to contextual cues associated with footshocks but did not change the dPAG electrical stimulation for freezing and escape responses. In a second experiment, lesion of the vPAG also did not change the amount of freezing and escape behavior produced by microinjections of semicarbazide into the dPAG. These findings indicate that freezing and escape defensive responses induced by dPAG stimulation do not depend on the integrity of the vPAG. A discussion on different neural circuitries that might underlie different inhibitory and active defensive behavioral patterns that animals display during threatening situations is presented.

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“…27), suggesting that the CeA is more directly connected with the behavioral output pathways responsible for fear responses. Although stimulation of areas that project to the LA have been used as an US to produce fear conditioning (28)(29)(30), this demonstration that direct stimulation of LA pyramidal neurons can serve as a reinforcement signal for fear learning is novel. A large number of studies have provided convincing evidence that associative plasticity in the LA contributes to fear memory formation (4,6,7).…”

Section: Discussionmentioning

confidence: 99%

Optical activation of lateral amygdala pyramidal cells instructs associative fear learning

Johansen¹,

Hamanaka²,

Monfils

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

279

207

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Humans and animals can learn that specific sensory cues in the environment predict aversive events through a form of associative learning termed fear conditioning. This learning occurs when the sensory cues are paired with an aversive event occuring in close temporal proximity. Activation of lateral amygdala (LA) pyramidal neurons by aversive stimuli is thought to drive the formation of these associative fear memories; yet, there have been no direct tests of this hypothesis. Here we demonstrate that viral-targeted, tissuespecific expression of the light-activated channelrhodopsin (ChR2) in LA pyramidal cells permitted optical control of LA neuronal activity. Using this approach we then paired an auditory sensory cue with optical stimulation of LA pyramidal neurons instead of an aversive stimulus. Subsequently presentation of the tone alone produced behavioral fear responses. These results demonstrate in vivo optogenetic control of LA neurons and provide compelling support for the idea that fear learning is instructed by aversive stimulus-induced activation of LA pyramidal cells.ear conditioning is a simple form of associative learning that provides a powerful model system to study associative plasticity and memory formation (1-4). During fear conditioning, a neutral stimulus [termed the conditioned stimulus (CS)], often an auditory tone, is paired repeatedly with an aversive stimulus [termed the unconditioned stimulus (US)] and animals learn that the CS predicts the occurrence of the US. When the CS is encountered after learning, animals emit a stereotyped group of adaptive responses, including behavioral freezing and associated physiological adjustments, which together are termed the fear response.The lateral nucleus of the amygdala (LA) is a site of associative plasticity, where US-evoked depolarization of LA pyramidal neurons is thought to instruct plasticity at synapses formed by CS inputs onto the same neurons (5-7). Several lines of indirect evidence support the idea that this plasticity occurs as a result of a Hebbian mechanism through which depolarization of LA pyramidal neurons by the shock US coincident with weaker activation of the same cells by auditory CS inputs results in fear learning (8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18). This hypothesis makes the strong prediction that pairing an auditory CS with direct activation of LA pyramidal neurons as an US should be sufficient, in the absence of a shock US, to support fear learning and memory formation. Here we tested this hypothesis by substituting the aversive US with optical stimulation (19,20) of LA pyramidal neurons during learning, and we report that physiological activation of these cells results in fear conditioning. ResultsThe light activated channelrhodopsin (ChR2) (19,20) has been used in other neural systems to activate specific cell populations and produce learning (21-23). We took advantage of this technology and targeted ChR2 to pyramidal cells by in vivo viralmediated gene transfer. We used an adeno-associated virus (AAV) to express a...

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Evidence of Pavlovian conditioned fear following electrical stimulation of the periaqueductal grey in the rat

Cited by 79 publications

References 39 publications

Signaled two-way avoidance learning using electrical stimulation of the inferior colliculus as negative reinforcement: effects of visual and auditory cues as warning stimuli

Signaled two-way avoidance learning using electrical stimulation of the inferior colliculus as negative reinforcement: effects of visual and auditory cues as warning stimuli

Lesion of the Ventral Periaqueductal Gray Reduces Conditioned Fear but Does Not Change Freezing Induced by Stimulation of the Dorsal Periaqueductal Gray

Optical activation of lateral amygdala pyramidal cells instructs associative fear learning

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