Selective reduction by dopamine of excitatory synaptic inputs to pyramidal neurons in primate prefrontal cortex

We have employed in vitro physiological methods to investigate dopaminergic modulation of excitatory synaptic transmission in monkey prefrontal cortex (PFC) circuits. We show that combined activation of D1‐like and D2‐like dopamine receptors results in the reduction of extracellular stimulation‐evoked isolated EPSCs in layer 3 pyramidal neurons. Using paired recordings from synaptically connected pyramidal neurons we have determined the basic properties of unitary synaptic connections between layer 3 pyramids in the primate PFC and, interestingly, we found that dopamine does not reduce synaptic transmission between nearby pairs of synaptically coupled PFC pyramidal neurons. This input specificity may be a critical aspect of the dopaminergic regulation of recurrent excitatory circuits in the PFC.

[1]  M. L. Pucak,et al.  Synaptic targets of pyramidal neurons providing intrinsic horizontal connections in monkey prefrontal cortex , 1998, The Journal of comparative neurology.

[2]  T. Sejnowski,et al.  Neurocomputational models of working memory , 2000, Nature Neuroscience.

[3]  P. Goldman-Rakic,et al.  Intrinsic circuit organization of the major layers and sublayers of the dorsolateral prefrontal cortex in the rhesus monkey , 1995, The Journal of comparative neurology.

[4]  D. Lewis,et al.  Horizontal synaptic connections in monkey prefrontal cortex: an in vitro electrophysiological study. , 2000, Cerebral cortex.

[5]  T. Sejnowski,et al.  Dopamine D1/D5 receptor modulation of excitatory synaptic inputs to layer V prefrontal cortex neurons. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[6]  D. Lewis,et al.  Parvalbumin‐immunoreactive axon terminals in macaque monkey and human prefrontal cortex: Laminar, regional, and target specificity of type I and type II synapses , 1999, The Journal of comparative neurology.

[7]  P. Goldman-Rakic,et al.  Modulation of memory fields by dopamine Dl receptors in prefrontal cortex , 1995, Nature.

[8]  J. B. Levitt,et al.  Patterns of intrinsic and associational circuitry in monkey prefrontal cortex , 1996, The Journal of comparative neurology.

[9]  T. Preuss.  Do Rats Have Prefrontal Cortex? The Rose-Woolsey-Akert Program Reconsidered , 1995, Journal of Cognitive Neuroscience.

[10]  German Barrionuevo,et al.  Synaptic targets of the intrinsic axon collaterals of supragranular pyramidal neurons in monkey prefrontal cortex , 2001, The Journal of comparative neurology.

[11]  T. Momiyama,et al.  Presynaptic dopamine D2‐like receptors inhibit excitatory transmission onto rat ventral tegmental dopaminergic neurones , 2000, The Journal of physiology.

[12]  P. Goldman-Rakic,et al.  Presynaptic regulation of recurrent excitation by D1 receptors in prefrontal circuits. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[13]  P. Goldman-Rakic,et al.  Regional, cellular, and subcellular variations in the distribution of D1 and D5 dopamine receptors in primate brain , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  B. Berger,et al.  Dopaminergic innervation of the cerebral cortex: unexpected differences between rodents and primates , 1991, Trends in Neurosciences.

[15]  Xiao-Jing Wang,et al.  A Model of Visuospatial Working Memory in Prefrontal Cortex: Recurrent Network and Cellular Bistability , 1998, Journal of Computational Neuroscience.

[16]  D. Law-Tho,et al.  Dopamine modulation of synaptic transmission in rat prefrontal cortex: an in vitro electrophysiological study , 1994, Neuroscience Research.

[17]  D. Henze,et al.  Dopamine increases excitability of pyramidal neurons in primate prefrontal cortex. , 2000, Journal of neurophysiology.

[18]  J. B. Levitt,et al.  Topography of pyramidal neuron intrinsic connections in macaque monkey prefrontal cortex (areas 9 and 46) , 1993, The Journal of comparative neurology.

[19]  P. Goldman-Rakic,et al.  Dopamine synaptic complex with pyramidal neurons in primate cerebral cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Patricia S. Goldman-Rakic,et al.  Quantitative Three-Dimensional Analysis of the Catecholaminergic Innervation of Identified Neurons in the Macaque Prefrontal Cortex , 1997, The Journal of Neuroscience.

[21]  H. E. Rosvold,et al.  Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. , 1979, Science.

[22]  S. Sesack,et al.  Chapter VI Dopamine systems in the primate brain , 1997 .

[23]  P. Goldman-Rakic,et al.  The role of D1-dopamine receptor in working memory: local injections of dopamine antagonists into the prefrontal cortex of rhesus monkeys performing an oculomotor delayed-response task. , 1994, Journal of neurophysiology.

[24]  K. Hikosaka,et al.  Increase of extracellular dopamine in primate prefrontal cortex during a working memory task. , 1997, Journal of neurophysiology.