Cerebral Cortex, Vol. 10, No. 12, 1168-1175,
December 2000
© 2000 Oxford University Press
Ventral Tegmental Area Afferents to the Prefrontal Cortex Maintain Membrane Potential ‘Up’ States in Pyramidal Neurons via D1 Dopamine Receptors
Center for Neuropharmacology and Neuroscience, Albany Medical College, Albany, NY 12208, USA
The electrophysiological nature of dopamine actions has been controversial for years, with data supporting both inhibitory and excitatory actions. In this study, we tested whether stimulation of the ventral tegmental area (VTA), the source of the dopamine innervation of the prefrontal cortex, would exert different responses depending on the membrane potential states that pyramidal neurons exhibit when recorded in vivo, and whether VTA stimulation would have a role in controlling transitions between these states. Prefrontal cortical neurons have a very negative resting membrane potential (down state) interrupted by plateau depolarizations (up state). Although the up state had been shown to be dependent on hippocampal afferents in nucleus accumbens neurons, our results indicate that neither hippocampal nor thalamic inputs are sufficient to drive up events in prefrontal cortical neurons. Electrical VTA stimulation resulted in a variety of actions, in many cases depending on the neuron membrane potential state. Trains of stimuli resembling burst firing evoked a long-lasting transition to the up state, an effect blocked by a D1 antagonist and mimicked by chemical VTA stimulation. These results indicate that projections from the VTA to the prefrontal cortex may be involved in controlling membrane potential states that define assemblies of activable pyramidal neurons in this region.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  N. K. B. Totah, Y. B. Kim, H. Homayoun, and B. Moghaddam Anterior Cingulate Neurons Represent Errors and Preparatory Attention within the Same Behavioral Sequence J. Neurosci., May 20, 2009; 29(20): 6418 - 6426. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 O. Valenti and A. A. Grace Entorhinal Cortex Inhibits Medial Prefrontal Cortex and Modulates the Activity States of Electrophysiologically Characterized Pyramidal Neurons In Vivo Cereb Cortex, March 1, 2009; 19(3): 658 - 674. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Y. Tseng, B. L. Lewis, T. Hashimoto, S. R. Sesack, M. Kloc, D. A. Lewis, and P. O'Donnell A Neonatal Ventral Hippocampal Lesion Causes Functional Deficits in Adult Prefrontal Cortical Interneurons J. Neurosci., November 26, 2008; 28(48): 12691 - 12699. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. L. Tierney, A. M. Thierry, J. Glowinski, J. M. Deniau, and Y. Gioanni Dopamine Modulates Temporal Dynamics of Feedforward Inhibition in Rat Prefrontal Cortex In Vivo Cereb Cortex, October 1, 2008; 18(10): 2251 - 2262. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Thurley, W. Senn, and H.-R. Luscher Dopamine Increases the Gain of the Input-Output Response of Rat Prefrontal Pyramidal Neurons J Neurophysiol, June 1, 2008; 99(6): 2985 - 2997. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. A. Milojkovic, W.-L. Zhou, and S. D. Antic Voltage and calcium transients in basal dendrites of the rat prefrontal cortex J. Physiol., December 1, 2007; 585(2): 447 - 468. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. C. Rotaru, D. A. Lewis, and G. Gonzalez-Burgos Dopamine D1 receptor activation regulates sodium channel-dependent EPSP amplification in rat prefrontal cortex pyramidal neurons J. Physiol., June 15, 2007; 581(3): 981 - 1000. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K.-Y. Tseng and P. O'Donnell Dopamine Modulation of Prefrontal Cortical Interneurons Changes during Adolescence Cereb Cortex, May 1, 2007; 17(5): 1235 - 1240. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Tu, S. Kroener, K. Abernathy, C. Lapish, J. Seamans, L. J. Chandler, and J. J. Woodward Ethanol Inhibits Persistent Activity in Prefrontal Cortical Neurons J. Neurosci., April 25, 2007; 27(17): 4765 - 4775. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Kepecs and S. Raghavachari Gating Information by Two-State Membrane Potential Fluctuations J Neurophysiol, April 1, 2007; 97(4): 3015 - 3023. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Durstewitz and T. Gabriel Dynamical Basis of Irregular Spiking in NMDA-Driven Prefrontal Cortex Neurons Cereb Cortex, April 1, 2007; 17(4): 894 - 908. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Chen, J. D. Bohanick, M. Nishihara, J. K. Seamans, and C. R. Yang Dopamine D1/5 Receptor-Mediated Long-Term Potentiation of Intrinsic Excitability in Rat Prefrontal Cortical Neurons: Ca2+-Dependent Intracellular Signaling J Neurophysiol, March 1, 2007; 97(3): 2448 - 2464. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. B. Floresco and M. T. Tse Dopaminergic Regulation of Inhibitory and Excitatory Transmission in the Basolateral Amygdala-Prefrontal Cortical Pathway J. Neurosci., February 21, 2007; 27(8): 2045 - 2057. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Nogueira, P. W. Kalivas, and A. Lavin Long-Term Neuroadaptations Produced by Withdrawal from Repeated Cocaine Treatment: Role of Dopaminergic Receptors in Modulating Cortical Excitability. J. Neurosci., November 22, 2006; 26(47): 12308 - 12313. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Kasanetz, L. A. Riquelme, P. O'Donnell, and M. G. Murer Turning off cortical ensembles stops striatal Up states and elicits phase perturbations in cortical and striatal slow oscillations in rat in vivo J. Physiol., November 15, 2006; 577(1): 97 - 113. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. Sun and G. V. Rebec Repeated cocaine self-administration alters processing of cocaine-related information in rat prefrontal cortex. J. Neurosci., July 26, 2006; 26(30): 8004 - 8008. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Lu, T. C. Jhou, and C. B. Saper Identification of Wake-Active Dopaminergic Neurons in the Ventral Periaqueductal Gray Matter J. Neurosci., January 4, 2006; 26(1): 193 - 202. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W.-X. Shi Slow Oscillatory Firing: A Major Firing Pattern of Dopamine Neurons in the Ventral Tegmental Area J Neurophysiol, November 1, 2005; 94(5): 3516 - 3522. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Lavin, L. Nogueira, C. C. Lapish, R. M. Wightman, P. E. M. Phillips, and J. K. Seamans Mesocortical Dopamine Neurons Operate in Distinct Temporal Domains Using Multimodal Signaling J. Neurosci., May 18, 2005; 25(20): 5013 - 5023. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. A. Milojkovic, M. S. Radojicic, and S. D. Antic A Strict Correlation between Dendritic and Somatic Plateau Depolarizations in the Rat Prefrontal Cortex Pyramidal Neurons J. Neurosci., April 13, 2005; 25(15): 3940 - 3951. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Bandyopadhyay, C. Gonzalez-Islas, and J. J. Hablitz Dopamine Enhances Spatiotemporal Spread of Activity in Rat Prefrontal Cortex J Neurophysiol, February 1, 2005; 93(2): 864 - 872. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Gonzalez-Burgos, L. S. Krimer, N. V. Povysheva, G. Barrionuevo, and D. A. Lewis Functional Properties of Fast Spiking Interneurons and Their Synaptic Connections With Pyramidal Cells in Primate Dorsolateral Prefrontal Cortex J Neurophysiol, February 1, 2005; 93(2): 942 - 953. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. V. Puig, F. Artigas, and P. Celada Modulation of the Activity of Pyramidal Neurons in Rat Prefrontal Cortex by Raphe Stimulation In Vivo: Involvement of Serotonin and GABA Cereb Cortex, January 1, 2005; 15(1): 1 - 14. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Y. Tseng and P. O'Donnell Post-pubertal Emergence of Prefrontal Cortical Up States Induced by D1-NMDA Co-activation Cereb Cortex, January 1, 2005; 15(1): 49 - 57. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. P. Battaglia, G. R. Sutherland, and B. L. McNaughton Hippocampal sharp wave bursts coincide with neocortical "up-state" transitions Learn. Mem., November 1, 2004; 11(6): 697 - 704. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. A. Milojkovic, M. S. Radojicic, t. l. P. S. Goldman-Rakic, and S. D. Antic Burst generation in rat pyramidal neurones by regenerative potentials elicited in a restricted part of the basilar dendritic tree J. Physiol., July 1, 2004; 558(1): 193 - 211. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Y. Tseng and P. O'Donnell Dopamine-Glutamate Interactions Controlling Prefrontal Cortical Pyramidal Cell Excitability Involve Multiple Signaling Mechanisms J. Neurosci., June 2, 2004; 24(22): 5131 - 5139. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. M. Brady and P. O'Donnell Dopaminergic Modulation of Prefrontal Cortical Input to Nucleus Accumbens Neurons In Vivo J. Neurosci., February 4, 2004; 24(5): 1040 - 1049. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. N. D. Kerr and D. Plenz Action Potential Timing Determines Dendritic Calcium during Striatal Up-States J. Neurosci., January 28, 2004; 24(4): 877 - 885. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. E. Young and C. R. Yang Dopamine D1/D5 Receptor Modulates State-Dependent Switching of Soma-Dendritic Ca2+ Potentials via Differential Protein Kinase A and C Activation in Rat Prefrontal Cortical Neurons J. Neurosci., January 7, 2004; 24(1): 8 - 23. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-M. Fellous and T. J. Sejnowski Regulation of Persistent Activity by Background Inhibition in an In Vitro Model of a Cortical Microcircuit Cereb Cortex, November 1, 2003; 13(11): 1232 - 1241. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. K. Seamans, L. Nogueira, and A. Lavin Synaptic Basis of Persistent Activity in Prefrontal Cortex In Vivo and in Organotypic Cultures Cereb Cortex, November 1, 2003; 13(11): 1242 - 1250. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. V. Puig, P. Celada, L. Diaz-Mataix, and F. Artigas In Vivo Modulation of the Activity of Pyramidal Neurons in the Rat Medial Prefrontal Cortex by 5-HT2A Receptors: Relationship to Thalamocortical Afferents Cereb Cortex, August 1, 2003; 13(8): 870 - 882. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. B. Floresco and A. A. Grace Gating of Hippocampal-Evoked Activity in Prefrontal Cortical Neurons by Inputs from the Mediodorsal Thalamus and Ventral Tegmental Area J. Neurosci., May 1, 2003; 23(9): 3930 - 3943. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Goto and P. O'Donnell Delayed Mesolimbic System Alteration in a Developmental Animal Model of Schizophrenia J. Neurosci., October 15, 2002; 22(20): 9070 - 9077. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. O'Donnell, B. L. Lewis, D. R. Weinberger, and B. K. Lipska Neonatal Hippocampal Damage Alters Electrophysiological Properties of Prefrontal Cortical Neurons in Adult Rats Cereb Cortex, September 1, 2002; 12(9): 975 - 982. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. J. Everitt and M. E. Wolf Psychomotor Stimulant Addiction: A Neural Systems Perspective J. Neurosci., May 1, 2002; 22(9): 3312 - 3320. [Full Text] [PDF]
|
|
|
|
|
|
A. E. Baldwin, K. Sadeghian, and A. E. Kelley Appetitive Instrumental Learning Requires Coincident Activation of NMDA and Dopamine D1 Receptors within the Medial Prefrontal Cortex J. Neurosci., February 1, 2002; 22(3): 1063 - 1071. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Degenetais, A.-M. Thierry, J. Glowinski, and Y. Gioanni Electrophysiological Properties of Pyramidal Neurons in the Rat Prefrontal Cortex: An In Vivo Intracellular Recording Study Cereb Cortex, January 1, 2002; 12(1): 1 - 16. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. McFarland and P. W. Kalivas The Circuitry Mediating Cocaine-Induced Reinstatement of Drug-Seeking Behavior J. Neurosci., November 1, 2001; 21(21): 8655 - 8663. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Goto and P. O'Donnell Network Synchrony in the Nucleus Accumbens In Vivo J. Neurosci., June 15, 2001; 21(12): 4498 - 4504. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Wang and P. O'Donnell D1 Dopamine Receptors Potentiate NMDA-mediated Excitability Increase in Layer V Prefrontal Cortical Pyramidal Neurons Cereb Cortex, May 1, 2001; 11(5): 452 - 462. [Abstract] [Full Text] [PDF]
|
|