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The Journal of Neuroscience, April 13, 2005, 25(15):3940-3951; doi:10.1523/JNEUROSCI.5314-04.2005

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Behavioral/Systems/Cognitive
A Strict Correlation between Dendritic and Somatic Plateau Depolarizations in the Rat Prefrontal Cortex Pyramidal Neurons

Bogdan A. Milojkovic,^1,2 Mihailo S. Radojicic,¹ and Srdjan D. Antic^1,3

¹Department of Neurobiology, Yale University, New Haven, Connecticut 06520-8001, ²Department of Neuroscience, Erasmus Medical Center, 3015 GE Rotterdam, The Netherlands, and ³Department of Neuroscience, University of Connecticut Health Center, Farmington, Connecticut 06030

One of the fundamental problems in neurobiology is to understand the cellular mechanism for sustained neuronal activity (neuronal UP states). Prefrontal pyramidal neurons readily switch to a long-lasting depolarized state after suprathreshold stimulation of basal dendrites. Analysis of the dendritic input-output function revealed that basal dendrites operate in a somewhat binary regimen (DOWN or UP) in regard to the amplitude of the glutamate-evoked electrical signal. Although the amplitude of the dendritic potential quickly becomes saturated (dendritic UP state), basal dendrites preserve their ability to code additional increase in glutamatergic input. Namely, after the saturation of the plateau amplitude, an additional increase in excitatory input is interpreted as an increase in plateau duration. Experiments performed in tetrodotoxin indicate that the maintenance of a stable depolarized state does not require inhibitory inputs to "balance" the excitation. In the absence of action potential-dependent (network-driven) GABAergic transmission, pyramidal neurons respond to brief (5 ms) glutamate pulses with stable long-lasting (500 ms) depolarizations. Voltage-sensitive dye recordings revealed that this somatic plateau depolarization is precisely time-locked with the regenerative dendritic plateau potential. The somatic plateau rises a few milliseconds after the onset of the dendritic transient and collapses with the breakdown of the dendritic plateau depolarization. In our in vitro model, the stable long-lasting somatic depolarization (UP state like) is a direct consequence of the local processing of a strong excitatory glutamatergic input arriving on the basal dendrite. The slow component of the somatic depolarization accurately mirrors the glutamate-evoked dendritic plateau potential (dendritic UP state).

Key words: basal dendrites; glutamate; voltage-sensitive dyes; dendritic recordings; plateau potentials; UP states

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Received June 1, 2004; revised February 20, 2005; accepted March 12, 2005.

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