Oncotarget

Research Papers:

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 and Jonathon Miller

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Oncotarget. 2018; 9:10016-10028. https://doi.org/10.18632/oncotarget.24245

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Abstract

Yuan-Hao Chen1, Tung-Tai Kuo2, Eagle Yi-Kung Huang3, Yu-Ching Chou4, Yung-Hsiao Chiang5, Barry J. Hoffer5,6 and Jonathon Miller6

1Department of Neurological Surgery, Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan, R.O.C

2Graduate Institute of Computer and Communication Engineering, National Taipei University of Technology, Taipei, Taiwan, R.O.C

3Department of Pharmacology, National Defense Medical Center, Taipei, Taiwan, R.O.C

4School of Public Health, National Defense Medical Center, Taipei, Taiwan, R.O.C

5Graduate Program on Neuroregeneration, Taipei Medical University, Taipei, Taiwan, R.O.C

6Department of Neurosurgery, Case Western Reserve University School of Medicine, Cleveland, Ohio, USA

Correspondence to:

Yuan-Hao Chen, email: [email protected]

Keywords: traumatic brain injury; dopamine; striatum; nicotine desensitization; nucleus accumbens shell

Received: November 03, 2017     Accepted: December 05, 2017     Published: January 13, 2018

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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