Effect of traumatic brain injury on nicotine-induced modulation of dopamine release in the striatum and nucleus accumbens shell

Yuan Hao Chen, Tung Tai Kuo, Eagle Yi Kung Huang, Yu Ching Chou, Yung Hsiao Chiang, Barry J. Hoffer, Jonathon Miller

Research output: Contribution to journalArticle

Abstract

Background: Traumatic brain injury is associated with substantial alterations in reward processing, but underlying mechanisms are controversial. Objective: A better understanding of alterations in dopamine (DA) release patterns from the dorsal striatum and nucleus accumbens shell (NAc) may provide insights into posttraumatic reward pathology. Materials and Methods: The patterns of DA release with or without exposure to nicotine in brain slices with striatum and NAc, isolated from Sprague-Dawley rats with 6 psi fluid percussion (FPI) or sham injury were analysis by using fast-scan cyclic voltammetry. Tonic and phasic DA releases were assessed using single pulse and 10 pulses at 25 Hz, respectively. DA release relative to stimulation intensity, frequency, number of pulses, and paired-pulse facilitation was evaluated to determine release probability and response to bursting. Results: There was a profound suppression in tonic DA release after nicotine desensitization after FPI, and the input/output curve for the DA release based on stimulation intensity was shifted to the right. FPI was associated with a significant decrease in frequency-dependent DA release augmentation, DA release induced by high frequency stimulation trains, and DA release in response to paired-pulse facilitation. The effect of nicotine desensitization was similar in FPI and sham-injured animals, although significantly smaller after FPI. Nicotine desensitization-induced differences between phasic and tonic release concentrations that contrasted with the reward-related signals then became less prominent in NAc after FPI. Conclusions: TBI blunts DA release from mesolimbic reward centers, and more intense stimuli are required to produce context-dependent DA release sufficient to have a physiological effect. Implications: The nicotine desensitization-related suppression in tonic DA release was profound with right-ward shift of the input/output curve for DA release after FPI. FPI was associated with a significant decrease in frequency-dependent DA release augmentation, DA release induced by high frequency stimulation trains, and DA release in response to paired-pulse facilitation. Nicotine desensitization-induced differences between phasic and tonic release concentrations that contrasted with the reward-related signals then became less prominent in NAc after FPI. TBI thus blunts DA release from mesolimbic reward centers, and more intense stimuli are required to produce context-dependent DA release sufficient to have a physiological effect.

LanguageEnglish
Pages10016-10028
Number of pages13
JournalOncotarget
Volume9
Issue number11
DOIs
StatePublished - Jan 1 2018

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Nucleus Accumbens
Nicotine
Dopamine
Percussion
Reward
Traumatic Brain Injury

Keywords

  • Dopamine
  • Nicotine desensitization
  • Nucleus accumbens shell
  • Striatum
  • Traumatic brain injury

ASJC Scopus subject areas

  • Oncology

Cite this

Chen, Y. H., Kuo, T. T., Huang, E. Y. K., Chou, Y. C., Chiang, Y. H., Hoffer, B. J., & Miller, J. (2018). Effect of traumatic brain injury on nicotine-induced modulation of dopamine release in the striatum and nucleus accumbens shell. Oncotarget, 9(11), 10016-10028. DOI: 10.18632/oncotarget.24245

Effect of traumatic brain injury on nicotine-induced modulation of dopamine release in the striatum and nucleus accumbens shell. / Chen, Yuan Hao; Kuo, Tung Tai; Huang, Eagle Yi Kung; Chou, Yu Ching; Chiang, Yung Hsiao; Hoffer, Barry J.; Miller, Jonathon.

In: Oncotarget, Vol. 9, No. 11, 01.01.2018, p. 10016-10028.

Research output: Contribution to journalArticle

Chen, Yuan Hao ; Kuo, Tung Tai ; Huang, Eagle Yi Kung ; Chou, Yu Ching ; Chiang, Yung Hsiao ; Hoffer, Barry J. ; Miller, Jonathon. / Effect of traumatic brain injury on nicotine-induced modulation of dopamine release in the striatum and nucleus accumbens shell. In: Oncotarget. 2018 ; Vol. 9, No. 11. pp. 10016-10028
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abstract = "Background: Traumatic brain injury is associated with substantial alterations in reward processing, but underlying mechanisms are controversial. Objective: A better understanding of alterations in dopamine (DA) release patterns from the dorsal striatum and nucleus accumbens shell (NAc) may provide insights into posttraumatic reward pathology. Materials and Methods: The patterns of DA release with or without exposure to nicotine in brain slices with striatum and NAc, isolated from Sprague-Dawley rats with 6 psi fluid percussion (FPI) or sham injury were analysis by using fast-scan cyclic voltammetry. Tonic and phasic DA releases were assessed using single pulse and 10 pulses at 25 Hz, respectively. DA release relative to stimulation intensity, frequency, number of pulses, and paired-pulse facilitation was evaluated to determine release probability and response to bursting. Results: There was a profound suppression in tonic DA release after nicotine desensitization after FPI, and the input/output curve for the DA release based on stimulation intensity was shifted to the right. FPI was associated with a significant decrease in frequency-dependent DA release augmentation, DA release induced by high frequency stimulation trains, and DA release in response to paired-pulse facilitation. The effect of nicotine desensitization was similar in FPI and sham-injured animals, although significantly smaller after FPI. Nicotine desensitization-induced differences between phasic and tonic release concentrations that contrasted with the reward-related signals then became less prominent in NAc after FPI. Conclusions: TBI blunts DA release from mesolimbic reward centers, and more intense stimuli are required to produce context-dependent DA release sufficient to have a physiological effect. Implications: The nicotine desensitization-related suppression in tonic DA release was profound with right-ward shift of the input/output curve for DA release after FPI. FPI was associated with a significant decrease in frequency-dependent DA release augmentation, DA release induced by high frequency stimulation trains, and DA release in response to paired-pulse facilitation. Nicotine desensitization-induced differences between phasic and tonic release concentrations that contrasted with the reward-related signals then became less prominent in NAc after FPI. TBI thus blunts DA release from mesolimbic reward centers, and more intense stimuli are required to produce context-dependent DA release sufficient to have a physiological effect.",
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N2 - Background: Traumatic brain injury is associated with substantial alterations in reward processing, but underlying mechanisms are controversial. Objective: A better understanding of alterations in dopamine (DA) release patterns from the dorsal striatum and nucleus accumbens shell (NAc) may provide insights into posttraumatic reward pathology. Materials and Methods: The patterns of DA release with or without exposure to nicotine in brain slices with striatum and NAc, isolated from Sprague-Dawley rats with 6 psi fluid percussion (FPI) or sham injury were analysis by using fast-scan cyclic voltammetry. Tonic and phasic DA releases were assessed using single pulse and 10 pulses at 25 Hz, respectively. DA release relative to stimulation intensity, frequency, number of pulses, and paired-pulse facilitation was evaluated to determine release probability and response to bursting. Results: There was a profound suppression in tonic DA release after nicotine desensitization after FPI, and the input/output curve for the DA release based on stimulation intensity was shifted to the right. FPI was associated with a significant decrease in frequency-dependent DA release augmentation, DA release induced by high frequency stimulation trains, and DA release in response to paired-pulse facilitation. The effect of nicotine desensitization was similar in FPI and sham-injured animals, although significantly smaller after FPI. Nicotine desensitization-induced differences between phasic and tonic release concentrations that contrasted with the reward-related signals then became less prominent in NAc after FPI. Conclusions: TBI blunts DA release from mesolimbic reward centers, and more intense stimuli are required to produce context-dependent DA release sufficient to have a physiological effect. Implications: The nicotine desensitization-related suppression in tonic DA release was profound with right-ward shift of the input/output curve for DA release after FPI. FPI was associated with a significant decrease in frequency-dependent DA release augmentation, DA release induced by high frequency stimulation trains, and DA release in response to paired-pulse facilitation. Nicotine desensitization-induced differences between phasic and tonic release concentrations that contrasted with the reward-related signals then became less prominent in NAc after FPI. TBI thus blunts DA release from mesolimbic reward centers, and more intense stimuli are required to produce context-dependent DA release sufficient to have a physiological effect.

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