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The Journal of Neurophysiology Vol. 83 No. 3 March 2000, pp. 1733-1750
Copyright ©2000 by the American Physiological Society
1Computational Neurobiology Laboratory, Howard Hughes Medical Institute, Salk Institute, La Jolla 92037; and 2Department of Biology, University of California San Diego, La Jolla, California 92093
Durstewitz, Daniel,
Jeremy K. Seamans, and
Terrence J. Sejnowski.
Dopamine-Mediated Stabilization of Delay-Period Activity in a
Network Model of Prefrontal Cortex. J. Neurophysiol. 83: 1733-1750, 2000. The prefrontal cortex (PFC) is
critically involved in working memory, which underlies memory-guided,
goal-directed behavior. During working-memory tasks, PFC neurons
exhibit sustained elevated activity, which may reflect the active
holding of goal-related information or the preparation of forthcoming
actions. Dopamine via the D1 receptor strongly modulates both this
sustained (delay-period) activity and behavioral performance in
working-memory tasks. However, the function of dopamine during
delay-period activity and the underlying neural mechanisms are only
poorly understood. Recently we proposed that dopamine might stabilize
active neural representations in PFC circuits during tasks involving
working memory and render them robust against interfering stimuli and
noise. To further test this idea and to examine the dopamine-modulated
ionic currents that could give rise to increased stability of neural
representations, we developed a network model of the PFC consisting of
multicompartment neurons equipped with Hodgkin-Huxley-like channel
kinetics that could reproduce in vitro whole cell and in vivo
recordings from PFC neurons. Dopaminergic effects on intrinsic ionic
and synaptic conductances were implemented in the model based on in
vitro data. Simulated dopamine strongly enhanced high, delay-type
activity but not low, spontaneous activity in the model network.
Furthermore the strength of an afferent stimulation needed to disrupt
delay-type activity increased with the magnitude of the
dopamine-induced shifts in network parameters, making the currently
active representation much more stable. Stability could be increased by
dopamine-induced enhancements of the persistent Na+
and N-methyl-D-aspartate (NMDA)
conductances. Stability also was enhanced by a reduction
in AMPA conductances. The increase in GABAA conductances
that occurs after stimulation of dopaminergic D1 receptors was
necessary in this context to prevent uncontrolled, spontaneous switches
into high-activity states (i.e., spontaneous activation of
task-irrelevant representations). In conclusion, the dopamine-induced
changes in the biophysical properties of intrinsic ionic and synaptic
conductances conjointly acted to highly increase stability of activated
representations in PFC networks and at the same time retain control
over network behavior and thus preserve its ability to adequately
respond to task-related stimuli. Predictions of the model can be tested
in vivo by locally applying specific D1 receptor, NMDA, or
GABAA antagonists while recording from PFC neurons in
delayed reaction-type tasks with interfering stimuli.
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