Functional uncoupling of inhibitory interneurons plays an important role in short-term sensitization of Aplysia gill and siphon withdrawal reflex.
نویسندگان
چکیده
Attempts to explain learning-associated potentiation of synaptic transmission in model systems such as withdrawal reflexes in the mollusk Aplysia or the hippocampus of vertebrates have focused on the mechanisms by which transmitter release is increased in the principal elements of the circuit. Increased transmission in neuronal networks such as the gill and siphon withdrawal reflex (GSWR) of Aplysia may, however, also be caused by a decrease of transmitter release by inhibitory interneurons. The importance and function of cholinergic inhibitory transmission in the GSWR network were investigated. Central application of the nicotinic cholinergic antagonist d-tubocurarine (d-TC) considerably potentiated gill contractions, evoked either by nerve stimulation or by tactile stimulation of the siphon. Compound EPSPs evoked in motoneurons upon siphon nerve stimulation were also significantly prolonged following application of d-TC, but were unaffected by hexamethonium, a blocker of excitatory ACh receptors in Aplysia. Recordings from excitatory interneurons showed that they received excitation followed by powerful inhibitory input upon stimulation of the siphon nerve. Application of d-TC completely blocked this rapid inhibition, thus prolonging the compound EPSPs evoked in the interneurons. These effects were obtained at a concentration of d-TC (100 microM) that almost totally blocked fast inhibitory cholinergic transmission, but was without effect on monosynaptic connections between sensory neurons and motoneurons of the reflex. Facilitation of (1) compound EPSCs in motoneurons and (2) evoked excitatory interneuronal firing was reduced in preparations already disinhibited by pretreatment with d-TC. Facilitation of sensory-motor synapses, however, was not reduced in the presence of d-TC, indicating that facilitatory interneurons are still activated under cholinergic blockade. These data show that transmission through the GSWR neuronal network is gated by a feedback inhibitory mechanism. They also suggest that a reduction of cholinergic inhibition onto excitatory interneurons may be a mechanism through which transmission within the GSWR network is increased during various forms of learning, such as sensitization. These data place new emphasis on the important role of inhibitory interneurons in determining the plastic properties of neuronal networks, in both invertebrates and vertebrates.
منابع مشابه
Monosynaptic connections made by the sensory neurons of the gill- and siphon-withdrawal reflex in Aplysia participate in the storage of long-term memory for sensitization.
We have found that in the gill- and siphon- withdrawal reflex of Aplysia, the memory for short-term sensitization grades smoothly into long-term memory with increased amounts of sensitization training. One cellular locus for the storage of the memory underlying short-term sensitization is the set of monosynaptic connections between the siphon sensory cells and the gill and siphon motor neurons....
متن کاملCutaneous activation of the inhibitory L30 interneurons provides a mechanism for regulating adaptive gain control in the siphon withdrawal reflex of Aplysia.
The functional role of inhibition in the neural network underlying the siphon withdrawal response (SWR) of Aplysia was assessed by examining a recurrent circuit comprised of identified inhibitory interneurons (L30s), and excitatory interneurons (L29s). We previously showed that activity-dependent potentiation of the L30 inhibitory synapse onto L29 can regulate the net excitatory input elicited ...
متن کاملDepletion of serotonin in the nervous system of Aplysia reduces the behavioral enhancement of gill withdrawal as well as the heterosynaptic facilitation produced by tail shock.
Noxious stimuli, such as electrical shocks to the animal's tail, enhance Aplysia's gill- and siphon-withdrawal reflex. Previous experimental work has indicated that this behavioral enhancement, known as dishabituation (if the reflex has been habituated) or sensitization (if it has not been habituated), might be mediated, at least in part, by the endogenous monoaminergic transmitter serotonin (5...
متن کاملLong-term sensitization in Aplysia increases the number of presynaptic contacts onto the identified gill motor neuron L7.
We have used the gill and siphon withdrawal reflex of Aplysia to study the morphological basis of the persistent synaptic plasticity that underlies long-term sensitization. One critical locus for storage of the memory for sensitization is the set of monosynaptic connections between identified siphon sensory neurons and gill and siphon motor neurons. To complement previous morphological studies ...
متن کاملIdentified serotonergic neurons LCB1 and RCB1 in the cerebral ganglia of Aplysia produce presynaptic facilitation of siphon sensory neurons.
Several lines of evidence suggest that 5-HT plays a significant role in presynaptic facilitation of the siphon sensory cells contributing to dishabituation and sensitization of the gill- and siphon-withdrawal reflex in Aplysia. Most recently, Glanzman et al. (1989) found that treatment with the 5-HT neurotoxin, 5,7-DHT markedly reduced both synaptic facilitation and behavioral dishabituation. T...
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ورودعنوان ژورنال:
- The Journal of neuroscience : the official journal of the Society for Neuroscience
دوره 13 5 شماره
صفحات -
تاریخ انتشار 1993