Elsevier

Physiology & Behavior

Volume 67, Issue 1, 1 August 1999, Pages 99-105
Physiology & Behavior

Articles
Amygdala Lesions Produce Analgesia in a Novel, Ethologically Relevant Acute Pain Test

https://doi.org/10.1016/S0031-9384(99)00042-6Get rights and content

Abstract

Acute pain tests using mechanical stimuli typically do not involve objects important in the evolutionary history of the subjects, and may fail to evaluate the contribution of biobehavioral defensive reactions to the total pain response. Spines are common structural defenses that protect plants and animals against predation. The present studies examined the reaction to contact with such natural, mechanical pain stimuli in the laboratory rat, utilizing a floor board with protruding pins located in the middle of a novel alley (the “fakir” test). Behavioral responses were characterized in 10-min tests (Experiment 1). Subjects showed voluntary contact with the pins followed by patterns of avoidance and risk assessment (stretch attend and stretch approach). Few subjects crossed the array of pins. The amygdala has been implicated in the perception of pain, particularly in stressful or fearful contexts. In Experiment 2, the fakir test was used to examine, concurrently, the effects of amygdala lesions on analgesiometric (frequency and duration of pin crossings) and anxiometric (risk assessment) measures. Large, bilateral, lesions of the amygdala significantly increased both the number of pin crossings and time spent on the pins without affecting the risk assessment measures. These findings suggest a possible dissociation between anxiety and pain perception with an important (nonaffective) role for the amygdala in the latter.

Section snippets

Experiment 1

In this study, rats were placed in an alley that had in its center an array of sharp pins embedded in a small platform. The size and spatial arrangement of the pins made it impossible for the rats to traverse the alley without making contact with the tips of the pins. There were no experimenter-imposed incentives for the rats to contact the pins, and the animals could move about freely. We predicted that rats would nevertheless make “voluntary” contacts with the pins because of their natural

Experiment 2

There is increasing evidence that nuclei in the area of the amygdala play a role in nociception. Electrophysiological recordings from cells in the amygdala following stimulation of peripheral pain fibers confirm that the amygdala receives nociceptive information (1). The amygdala receives direct projections from the regions of the thalamus 20, 28 and parabrachial nucleus (27) that are innervated by pain pathways 18, 19, 22. Behavioral results following amygdala manipulations have been mixed,

Summary

The present study presented a novel pain test involving the exposure of rats to acute, mechanical pain producing stimuli of a punctate nature in a context conducive to the expression of a range of behavioral responses to this ethologically relevant class of painful stimuli. Although there were no experimenter-imposed incentives to contact the pins, rats exhibited a pattern of risk assessment that involved high levels of voluntary tactile exploration of the painful objects. Amygdala lesions

References (36)

  • J.K. Shepherd et al.

    The anxiety/defense test batteryInfluence of gender and ritanserin treatment on antipredator defensive behavior

    Physiol. Behav.

    (1992)
  • J.F. Bernard et al.

    The spino(trigemino)pontoamygdaloid pathwayElectrophysiological evidence for an involvement in pain processes

    J. Neurophysiol.

    (1990)
  • D.C. Blanchard et al.

    Innate and conditioned reactions to threat in rats with amygdaloid lesions

    J. Comp. Physiol. Psychol.

    (1972)
  • D.C. Blanchard et al.

    Risk assessment and animal models of anxiety

    (1991)
  • D.C. Blanchard et al.

    Diazepam alters risk assessment in an anxiety/defense test battery

    Psychopharmacology (Berlin)

    (1990)
  • R.J. Blanchard et al.

    Anti-predator defensive behaviors in a visible burrow system

    J. Comp. Psychol.

    (1989)
  • R.J. Blanchard et al.

    Escape and avoidance responses to a fear-eliciting stimulus

    Psychonom. Sci.

    (1968)
  • L Bourgeais et al.

    Projections from the nociceptive responding area of the central nucleus of the amygdalaA PHA-L study in the rat

    Soc. Neurosci. Abstr.

    (1997)
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