Long‐lasting Potentiation of a Direct Central Connection between Identified Motor Neurons in the Locust

Abstract

The plasticity of the direct central connection between the fast extensor and the posterior fast flexor tibiae motor neurons in the locust (Schistocerca gregaria) metathoracic ganglion was studied. An action potential in the fast extensor results in a monosynaptic excitatory postsynaptic potential (EPSP) in the flexor motor neuron. Antidromic stimulation of the fast extensor at 100 Hz for 3.5 s resulted in a long-lasting potentiation of the EPSP amplitude. The potentiation was not dependent on feedback caused by movement of the tibia, and was associated with an increase in the input resistance of the flexor motor neuron. The potentiation was heterosynaptic, and was not affected by bath application of the N-methyl-D-aspartate receptor antagonist 2-amino-5-phosphonovaleric acid. The potentiation was voltage dependent, as hyperpolarizing the flexor motor neuron during the stimulation blocked the development of the potentiation whereas depolarizing the flexor in the absence of presynaptic activity caused potentiation of subsequent fast extensor-evoked EPSPs. The depolarization-induced potentiation was calcium dependent. Antidromic stimulation of the fast extensor at 100 Hz for 3.5 s also caused modulation of the presynaptic action potential. The spike duration was increased and the amplitude of the afterhyperpolarization reduced. These effects were dependent on movement of the tibia. Bath application of the 5-hydroxytryptamine (5-HT) receptor antagonist ketanserin blocked the changes in the presynaptic spike. The modulation was probably due to the release of 5-HT from proprioceptive afferents that monitor movement of the tibia about the femur. The modulation of the presynaptic action potential increases transmitter release onto the flexor motor neurons, and this acts in synergy with the postsynaptic modulation to potentiate the connection.

The activity‐dependent plasticity of segmental and intersegmental synaptic connections in the lamprey spinal cord

“…Individual neurons can often evoke different forms of plasticity at output synapses onto two or more postsynaptic targets (Katz et al . 1993; Parker, 1995a; Markram et al . 1998; references therein).…”

“…1993; Le Ray & Cattaert, 1999) and nonrhythmic motor outputs (Atwood et al . 1994; Parker, 1995a,1b; Byrne & Kandel, 1996), little attention has focused on the role of activity‐dependent synaptic plasticity in patterning rhythmic network activity.…”

“…1998 and references therein) has shown that specific cellular and synaptic effects cannot simply be extrapolated to other neurons or synapses. Of particular relevance to this study is the fact that the properties of inputs made by a single presynaptic neuron can differ markedly when examined in different postsynaptic targets (see Parker, 1995a; Markram et al . 1998, and references therein).…”

Active Motor Neurons Potentiate Their Own Sensory Inputs via Glutamate-Induced Long-Term Potentiation

“…• Previous studies on both vertebrate and invertebrate models put forward the idea that LTP induction may require highfrequency discharge of the participating neurons (Artola and Singer, 1987;Parker, 1995;Bao et al, 1997). However, the intracellular or extracellular stimulation frequencies used in our experiments never exceeded 15 Hz, which corresponds to the low physiological spiking frequencies observed during locomotor behavior.…”

“…The long-lasting enhancement of synaptic efficacy, so called long-term potentiation (LTP), has been studied extensively in the mammalian brain structures (Gustafsson and Wigström, 1988;White et al, 1988;Zalutsky and Nicoll, 1990;Isaac et al, 1995). Long-term changes also have been described in various neuronal networks and especially in invertebrate motor systems such as in Aplysia (Castellucci et al, 1978;Dale et al, 1988) and the locust (Parker, 1995).…”