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Journal of Neuroscience, Vol 15, 3622-3639, Copyright © 1995 by Society for Neuroscience
Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input
P O'Donnell and AA Grace
Department of Neuroscience, University of Pittsburgh, Pennsylvania 15260, USA.
The interactions among excitatory inputs arising from the prefrontal
cortex, amygdala, and hippocampus, and innervating nucleus accumbens
neurons were studied using in vivo intracellular recording techniques.
Neurons recorded in the accumbens displayed one of three activity states:
(1) silent, (2) spontaneously firing at low, constant rates, or (3) a
bistable membrane potential, characterized by alternating periods of
activity and silence occurring in concert with spontaneous transitions
between two steady-state membrane potentials (average, - 77.3 +/- 7.1 mV
base, -63.0 +/- 7.4 mV plateau). These neurons also exhibited a high degree
of convergence of responses elicited by stimulation of each of the three
excitatory inputs tested. Activation of hippocampal afferents, but not
cortical, amygdaloid, or thalamic afferents, induced bistable cells to
switch to the depolarized (active) state. In contrast, no bistable cells
were encountered in the nucleus accumbens following an acute transection of
the fornix. Furthermore, microinjection of lidocaine in the vicinity of the
hippocampal afferents at the level of the fornix caused a reversible
elimination of the plateau phase in bistable cells. These data suggest that
hippocampal input is necessary for accumbens neurons to enter a
depolarized, active state. Furthermore, activation of prefrontal cortical
inputs fail to evoke spike firing in accumbens neurons unless they are in
this active state. Consequently, the hippocampus appears to be capable of
gating prefrontal corticoaccumbens throughput.
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