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The Journal of Neuroscience, August 2, 2006, 26(31):8148-8159; doi:10.1523/JNEUROSCI.0723-06.2006

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Behavioral/Systems/Cognitive
Inverted-U Profile of Dopamine–NMDA-Mediated Spontaneous Avalanche Recurrence in Superficial Layers of Rat Prefrontal Cortex

Craig V. Stewart and Dietmar Plenz

Unit of Neural Network Physiology, Laboratory of Systems Neuroscience, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland 20892

Correspondence should be addressed to Dr. Dietmar Plenz, Unit of Neural Network Physiology, Laboratory of Systems Neuroscience, Porter Neuroscience Research Center, National Institute of Mental Health, National Institutes of Health, Room 3A-100, 35 Convent Drive, Bethesda, MD 20892. Email: plenzd{at}mail.nih.gov

Prefrontal cortex (PFC) functions, such as working memory, attention selection, and memory retrieval, depend critically on dopamine and NMDA receptor activation by way of an inverted-U-shaped pharmacological profile. Although single neuron responses in the PFC have shown some aspects of this profile, a network dynamic that follows the dopamine–NMDA dependence has not been identified.

We studied neuronal network activity in acute medial PFC slices of adult rats by recording local field potentials (LFPs) with microelectrode arrays. Bath application of dopamine or the dopamine D₁ agonist SKF38393 [(+/–)-1-phenyl-2,3,4,5-tetrahydro-(1H)-3-benzazepine-7,8-diol hydrochloride] in combination with NMDA induced spontaneous LFPs predominantly in superficial cortex layers. The LFPs at single electrodes were characterized by sharp negative peaks that were clustered in time across electrodes revealing diverse spatiotemporal patterns on the array. The pattern formation required fast GABAergic transmission, coactivation of the dopamine D₁ and NMDA receptor, and depended in an inverted-U profile on dopamine. At moderate concentrations of dopamine or the dopamine D₁ agonist, the pattern size distribution formed a power law with exponent = –1.5, indicating that patterns are organized in the form of neuronal avalanches, thereby maximizing spatial correlations in the network. At lower or higher concentrations, was more negative than –1.5, indicating reduced spatial correlations. Likewise, at moderate dopamine concentrations, the avalanche rate and recurrence of specific avalanches was maximal with recurrence frequencies after a "power law"-like heavy-tail distribution with a slope of –2.4.

We suggest that the dopamine–NMDA-dependent spontaneous recurrence of specific avalanches in superficial cortical layers might facilitate integrative and associative aspects of PFC functions.

Key words: prefrontal cortex; spontaneous activity; dopamine; NMDA; spatiotemporal activity patterns; microelectrode array; acute slice; local field potential

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Received Feb. 17, 2006; revised June 30, 2006; accepted July 5, 2006.

Correspondence should be addressed to Dr. Dietmar Plenz, Unit of Neural Network Physiology, Laboratory of Systems Neuroscience, Porter Neuroscience Research Center, National Institute of Mental Health, National Institutes of Health, Room 3A-100, 35 Convent Drive, Bethesda, MD 20892. Email: plenzd{at}mail.nih.gov

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