Reward-Induced Phasic Dopamine Release in the Monkey Ventral Striatum and Putamen

In-vivo voltammetry has successfully been used to detect dopamine release in rodent brains, but its application to monkeys has been limited. We have previously detected dopamine release in the caudate of behaving Japanese monkeys using diamond microelectrodes (Yoshimi 2011); however it is not known whether the release pattern is the same in various areas of the forebrain. Recent studies have suggested variations in the dopaminergic projections to forebrain areas. In the present study, we attempted simultaneous recording at two locations in the striatum, using fast-scan cyclic voltammetry (FSCV) on carbon fibers, which has been widely used in rodents. Responses to unpredicted food and liquid rewards were detected repeatedly. The response to the liquid reward after conditioned stimuli was enhanced after switching the prediction cue. These characteristics were generally similar between the ventral striatum and the putamen. Overall, the technical application of FSCV recording in multiple locations was successful in behaving primates, and further voltammetric recordings in multiple locations will expand our knowledge of dopamine reward responses.

[1]  Diane R. Eaker,et al.  Development of the Mayo Investigational Neuromodulation Control System: toward a closed-loop electrochemical feedback system for deep brain stimulation. , 2013, Journal of neurosurgery.

[2]  R. M. Wightman,et al.  Real-time characterization of dopamine overflow and uptake in the rat striatum , 1988, Neuroscience.

[3]  P. Phillips,et al.  Dopamine Encoding of Pavlovian Incentive Stimuli Diminishes with Extended Training , 2013, The Journal of Neuroscience.

[4]  W. Schultz,et al.  Monitoring extracellular pH, oxygen, and dopamine during reward delivery in the striatum of primates , 2012, Front. Behav. Neurosci..

[5]  John L. Hudson,et al.  In Vivo Electrochemical Studies of Dopamine Overflow and Clearance in the Striatum of Normal and MPTP‐Treated Rhesus Monkeys , 1996, Journal of neurochemistry.

[6]  R. Wightman,et al.  Response times of carbon fiber microelectrodes to dynamic changes in catecholamine concentration. , 2002, Analytical chemistry.

[7]  John A. Dani,et al.  Controls of Tonic and Phasic Dopamine Transmission in the Dorsal and Ventral Striatum , 2009, Molecular Pharmacology.

[8]  A. Siapas,et al.  Dopamine Signaling Differences in the Nucleus Accumbens and Dorsal Striatum Exploited by Nicotine , 2009, The Journal of Neuroscience.

[9]  Nao Chuhma,et al.  Dopamine Neurons Control Striatal Cholinergic Neurons via Regionally Heterogeneous Dopamine and Glutamate Signaling , 2014, Neuron.

[10]  A. Graybiel.  Habits, rituals, and the evaluative brain. , 2008, Annual review of neuroscience.

[11]  O. Hikosaka,et al.  A possible role of midbrain dopamine neurons in short- and long-term adaptation of saccades to position-reward mapping. , 2004, Journal of neurophysiology.

[12]  Ziv M. Williams,et al.  Electrical Stimulation-Evoked Dopamine Release in the Primate Striatum , 2013, Stereotactic and Functional Neurosurgery.

[13]  Young-Min Shon,et al.  High frequency stimulation of the subthalamic nucleus evokes striatal dopamine release in a large animal model of human DBS neurosurgery. , 2010 .

[14]  R. Wightman,et al.  Real-time measurement of dopamine fluctuations after cocaine in the brain of behaving rats. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Andrew R. Mitz,et al.  Real-Time Dopamine Measurement in Awake Monkeys , 2014, PloS one.

[16]  Aneesha Badrinarayan,et al.  Aversive Stimuli Differentially Modulate Real-Time Dopamine Transmission Dynamics within the Nucleus Accumbens Core and Shell , 2012, The Journal of Neuroscience.

[17]  B. J. Venton,et al.  Subsecond detection of physiological adenosine concentrations using fast-scan cyclic voltammetry. , 2007, Analytical chemistry.

[18]  J. J. Cone,et al.  Primary food reward and reward‐predictive stimuli evoke different patterns of phasic dopamine signaling throughout the striatum , 2011, The European journal of neuroscience.

[19]  W. Schultz,et al.  Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  S. Kitazawa,et al.  Subsecond reward-related dopamine release in the mouse dorsal striatum , 2009, Neuroscience Research.

[21]  S. Kitazawa,et al.  Phasic reward responses in the monkey striatum as detected by voltammetry with diamond microelectrodes , 2011, Neuroscience Research.

[22]  K. Yoshimi,et al.  Temporal differentiation of pH-dependent capacitive current from dopamine. , 2014, Analytical chemistry.

[23]  N. Logothetis,et al.  A combined MRI and histology atlas of the rhesus monkey brain in stereotaxic coordinates , 2007 .

[24]  J. Roeper.  Dissecting the diversity of midbrain dopamine neurons , 2013, Trends in Neurosciences.

[25]  H. Okano,et al.  Possibility for neurogenesis in substantia nigra of parkinsonian brain , 2005 .

[26]  E. Vaadia,et al.  Midbrain Dopaminergic Neurons and Striatal Cholinergic Interneurons Encode the Difference between Reward and Aversive Events at Different Epochs of Probabilistic Classical Conditioning Trials , 2008, The Journal of Neuroscience.

[27]  S. Cragg,et al.  Dopamine release in the basal ganglia , 2011, Neuroscience.

[28]  W. Schultz.  Behavioral dopamine signals , 2007, Trends in Neurosciences.

[29]  P. Garris,et al.  Simultaneous dopamine and single-unit recordings reveal accumbens GABAergic responses: implications for intracranial self-stimulation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[30]  O. Hikosaka,et al.  Two types of dopamine neuron distinctly convey positive and negative motivational signals , 2009, Nature.

[31]  T. Robbins,et al.  Putting a spin on the dorsal–ventral divide of the striatum , 2004, Trends in Neurosciences.

[32]  S. Nakanishi,et al.  Aversive behavior induced by optogenetic inactivation of ventral tegmental area dopamine neurons is mediated by dopamine D2 receptors in the nucleus accumbens , 2014, Proceedings of the National Academy of Sciences.

[33]  A. Björklund,et al.  Dopamine neuron systems in the brain: an update , 2007, Trends in Neurosciences.

[34]  O. Hornykiewicz,et al.  Effect of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine on the regional distribution of brain monoamines in the rhesus monkey , 1991, Neuroscience.

[35]  R. Wightman,et al.  Differential dopamine release dynamics in the nucleus accumbens core and shell track distinct aspects of goal-directed behavior for sucrose , 2012, Neuropharmacology.