Behavioral, central monoaminergic and hypothalamo-pituitary-adrenal axis correlates of fear-conditioned analgesia in rats

Neuroscience. 2006;138(4):1309-17. doi: 10.1016/j.neuroscience.2005.11.063. Epub 2006 Jan 19.

Abstract

Fear-conditioned analgesia is an important survival response which is expressed upon re-exposure to a context previously paired with a noxious stimulus. The aim of the present study was to characterize further the behavioral, monoaminergic and hypothalamo-pituitary-adrenal axis alterations associated with expression of fear-conditioned analgesia. Rats which had received footshock conditioning 24 h earlier, exhibited reduced formalin-evoked nociceptive behavior upon re-exposure to the footshock chamber, compared with non-footshocked formalin-treated rats. Intra-plantar injection of formalin reduced the duration of contextually-induced freezing and 20-40 kHz ultrasound emission. Intra-plantar injection of formalin to non-footshocked, non-conditioned rats did not induce ultrasonic vocalizations. Intra-plantar injection of formalin to footshock-conditioned rats, significantly increased tissue levels of 3,4-dihydroxyphenylacetic acid and the 3,4-dihydroxyphenylacetic acid:dopamine ratio in the periaqueductal gray and reduced levels of dopamine in the thalamus, compared with saline-treated footshocked controls. Non-footshocked, non-conditioned rats were capable of mounting a robust formalin-evoked increase in plasma corticosterone levels. Moreover, plasma corticosterone levels were significantly higher in saline-treated, footshock conditioned rats compared with saline-treated non-footshocked rats and levels did not differ between saline- and formalin-treated footshock conditioned rats. Assessment of the effects of the intra-plantar injection procedure revealed an attenuation of short-term extinction of contextually-induced freezing in rats anesthetized for intra-plantar injection of saline compared with non-anesthetized, non-injected rats as well as discrete effects on monoamines, their metabolites and plasma corticosterone levels. These data extend behavioral characterization of the phenomenon of fear-conditioned analgesia and suggest that measurement of ultrasound emission may be used as an ethologically relevant index of the defense response during fear-conditioned analgesia. Ultrasonic vocalization may also be a useful behavioral output to aid separation of nociception and aversion. The data provide evidence for discrete alterations in dopaminergic activity in the periaqueductal gray and thalamus and for altered hypothalamo-pituitary-adrenal axis activity following expression of defensive behavior.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3,4-Dihydroxyphenylacetic Acid / metabolism
  • Analgesia
  • Animals
  • Behavior, Animal / physiology
  • Biogenic Monoamines / metabolism*
  • Brain / metabolism
  • Conditioning, Psychological
  • Corticosterone / blood
  • Disease Models, Animal
  • Dopamine / metabolism
  • Electric Stimulation / adverse effects
  • Fear / physiology*
  • Hypothalamo-Hypophyseal System / metabolism*
  • Male
  • Neural Pathways / metabolism
  • Pain / metabolism*
  • Pain / physiopathology
  • Pain Measurement / drug effects
  • Pain Threshold / drug effects
  • Pain Threshold / physiology*
  • Pituitary-Adrenal System / metabolism*
  • Rats
  • Stress, Psychological / metabolism
  • Stress, Psychological / physiopathology
  • Vocalization, Animal / drug effects
  • Vocalization, Animal / physiology

Substances

  • Biogenic Monoamines
  • 3,4-Dihydroxyphenylacetic Acid
  • Dopamine
  • Corticosterone