A microdialysis study of nucleus accumbens core and shell dopamine during operant responding in the rat

This investigation examined dopamine release and metabolism in nucleus accumbens core and shell during three operant tasks in the rat. Rats were trained to lever press on a fixed-ratio 5, variable-interval 30 s, or a tandem variable interval 30/fixed-ratio 5 schedules; these three schedules were chosen because they generate a wide range of response and reinforcement rates. After several weeks of training, dialysis probes were implanted into nucleus accumbens core or shell subregions. A single 30 min behavioural session was conducted during the dialysis test session. Rats lever pressing on each of the three operant schedules showed a significant increase in extracellular dopamine relative to the food-deprived control group during the behavioural session. In addition, increases in dopamine in nucleus accumbens shell were found to be significantly greater than in the core during the lever pressing period. Across all three schedules, extracellular dopamine in the nucleus accumbens was significantly correlated with the number of lever presses performed, but was not correlated with the number of food pellets delivered. Analysis of covariance, which used amount of food consumed as the covariate, showed an overall group difference, indicating that dopamine levels increased in lever pressing animals even if one corrected for the amount of food consumed. These results indicate that dopamine release was more responsive in the nucleus accumbens shell than in the core during operant responding, and that increases in extracellular dopamine in nucleus accumbens are related to response rate rather than reinforcement magnitude.

[1]  Anders Björklund,et al.  Regional differences in the regulation of dopamine and noradrenaline release in medial frontal cortex, nucleus accumbens and caudate-putamen: a microdialysis study in the rat , 1992, Brain Research.

[2]  L. Pellegrino,et al.  stereotaxic atlas of the rat brain , 1967 .

[3]  John D. Salamone,et al.  The role of brain dopamine in response initiation: effects of haloperidol and regionally specific dopamine depletions on the local rate of instrumental responding , 1993, Brain Research.

[4]  J. González-Mora,et al.  Changes in monoamine turnover in forebrain areas associated with masculine sexual behavior: a microdialysis study , 1994, Brain Research.

[5]  D. S. Zahm,et al.  On the significance of subterritories in the “accumbens” part of the rat ventral striatum , 1992, Neuroscience.

[6]  D. S. Zahm,et al.  Two transpallidal pathways originating in the rat nucleus accumbens , 1990, The Journal of comparative neurology.

[7]  Functional and anatomical evidence for different dopamine dynamics in the core and shell of the nucleus accumbens in slices of rat brain , 1996, Synapse.

[8]  T. Ono,et al.  Neuronal activity in the ventral tegmental area (VTA) during motivated bar press feeding in the monkey , 1987, Brain Research.

[9]  A. Imperato,et al.  Changes in brain dopamine and acetylcholine release during and following stress are independent of the pituitary-adrenocortical axis , 1991, Brain Research.

[10]  A. Louilot,et al.  Asymmetrical involvement of mesolimbic dopaminergic neurons in affective perception , 1995, Neuroscience.

[11]  Peter W. Kalivas,et al.  Selective activation of dopamine transmission in the shell of the nucleus accumbens by stress , 1995, Brain Research.

[12]  M. Kreifeldt,et al.  Modulation of locomotor activity by NMDA receptors in the nucleus accumbens core and shell regions of the rat , 1994, Brain Research.

[13]  J. Salamone,et al.  The Role of Accumbens Dopamine in Lever Pressing and Response Allocation: Effects of 6-OHDA Injected into Core and Dorsomedial Shell , 1998, Pharmacology Biochemistry and Behavior.

[14]  A. Deutch,et al.  Pharmacological characterization of dopamine systems in the nucleus accumbens core and shell , 1992, Neuroscience.

[15]  H. Fibiger,et al.  Feeding-evoked dopamine release in the nucleus accumbens: regulation by glutamatergic mechanisms , 1997, Neuroscience.

[16]  A. Gratton,et al.  Electrochemical monitoring of extracellular dopamine in nucleus accumbens of rats lever-pressing for food , 1994, Brain Research.

[17]  H. Groenewegen,et al.  Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat , 1992, The Journal of comparative neurology.

[18]  A. Björklund,et al.  Transmitter release from transplants of fetal ventral mesencephalon or locus coeruleus in the rat frontal cortex and nucleus accumbens: effects of pharmacological and behaviorally activating stimuli , 1994, Brain Research.

[19]  J. Salamone,et al.  Involvement of nucleus accumbens dopamine in the motor activity induced by periodic food presentation: a microdialysis and behavioral study , 1992, Brain Research.

[20]  H. Groenewegen,et al.  Compartmental distribution of ventral striatal neurons projecting to the mesencephalon in the rat , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  Akira Tsuda,et al.  Eating and drinking cause increased dopamine release in the nucleus accumbens and ventral tegmental area in the rat: Measurement by in vivo microdialysis , 1992, Neuroscience Letters.

[22]  J. Salamone,et al.  The role of nucleus accumbens dopamine in responding on a continuous reinforcement operant schedule: A neurochemical and behavioral study , 1993, Pharmacology Biochemistry and Behavior.

[23]  H. Groenewegen,et al.  Morphological differences between projection neurons of the core and shell in the nucleus accumbens of the rat , 1992, Neuroscience.

[24]  J. Salamone,et al.  Nucleus accumbens dopamine release increases during instrumental lever pressing for food but not free food consumption , 1994, Pharmacology Biochemistry and Behavior.

[25]  J. Salamone The behavioral neurochemistry of motivation: methodological and conceptual issues in studies of the dynamic activity of nucleus accumbens dopamine , 1996, Journal of Neuroscience Methods.

[26]  B. Hoebel,et al.  Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by microdialysis. , 1988, Life sciences.

[27]  R. Roth,et al.  Selective Increase in Dopamine Utilization in the Shell Subdivision of the Nucleus Accumbens by the Benzodiazepine Inverse Agonist FG 7142 , 1995, Journal of neurochemistry.

[28]  A. Kelley,et al.  Glutamate receptors in the nucleus accumbens shell control feeding behavior via the lateral hypothalamus , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  J. Chapin,et al.  Behavioral associations of neuronal activity in the ventral tegmental area of the rat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  A. Phillips,et al.  Sexual behavior increases dopamine transmission in the nucleus accumbens and striatum of male rats: comparison with novelty and locomotion. , 1992 .

[31]  A. Gratton,et al.  Behavior-Relevant Changes in Nucleus Accumbens Dopamine Transmission Elicited by Food Reinforcement: An Electrochemical Study in Rat , 1996, The Journal of Neuroscience.

[32]  J. Salamone,et al.  A neurochemical and behavioral investigation of the involvement of nucleus accumbens dopamine in instrumental avoidance , 1993, Neuroscience.

[33]  E. Abercrombie,et al.  Differential Effect of Stress on In Vivo Dopamine Release in Striatum, Nucleus Accumbens, and Medial Frontal Cortex , 1989, Journal of neurochemistry.

[34]  P. Mermelstein,et al.  Increased extracellular dopamine in the nucleus accumbens and striatum of the female rat during paced copulatory behavior. , 1995, Behavioral neuroscience.

[35]  P. Kalivas,et al.  The relationship between MRNA levels and the locomotor response to novelty , 1994, Brain Research.

[36]  H. Fibiger,et al.  Dopaminergic correlates of motivated behavior: importance of drive , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.