The Journal of Neuroscience, March 1, 1999, 19(5):1863-1875
GABAergic Excitatory Synapses and Electrical Coupling Sustain
Prolonged Discharges in the Prey Capture Neural Network of Clione
limacina
Tigran P.
Norekian
Department of Biology, Arizona State University, Tempe, Arizona
85287-1501, and Friday Harbor Laboratories, University of Washington,
Friday Harbor, Washington 98250
Afterdischarges represent a prominent characteristic of the neural
network that controls prey capture reactions in the carnivorous mollusc
Clione limacina. Their main functional implication is transformation of a brief sensory input from a prey into a lasting prey
capture response. The present study, which focuses on the neuronal
mechanisms of afterdischarges, demonstrates that a single pair of
interneurons [cerebral A interneuron (Cr-Aint)] is responsible for
afterdischarge generation in the network. Cr-Aint neurons are
electrically coupled to all other neurons in the network and produce
slow excitatory synaptic inputs to them. This excitatory transmission
is found to be GABAergic, which is demonstrated by the use of GABA
antagonists, uptake inhibitors, and double-labeling experiments showing
that Cr-Aint neurons are GABA-immunoreactive. The Cr-Aint neurons
organize three different pathways in the prey capture network, which
provide positive feedback necessary for sustaining prolonged spike
activity. The first pathway includes electrical coupling and slow
chemical transmission from the Cr-Aint neurons to all other neurons in
the network. The second feedback is based on excitatory reciprocal
connections between contralateral interneurons. Recurrent excitation
via the contralateral cell can sustain prolonged interneuron firing,
which then drives the activity of all other cells in the network. The
third positive feedback is represented by prominent afterdepolarizing
potentials after individual spikes in the Cr-Aint neurons.
Afterdepolarizations apparently represent recurrent GABAergic
excitatory inputs. It is suggested here that these afterdepolarizing
potentials are produced by GABAergic excitatory autapses.
Key words:
recurrent inputs; autapses; afterdepolarization; afterdischarge; positive feedback; neural network; mollusc; feeding; GABAergic interneuron; GABA immunoreactivity
Copyright © 1999 Society for Neuroscience 0270-6474/99/1951863-13$05.00/0
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