Competition regulates the efficacy of an identified synapse in crickets

Abstract

The efficacy of the synaptic contact between an identified sensory neuron and an identified interneuron in crickets is increased when neighboring afferent synapses are removed early in postembryonic life. The physiological changes are correlated with changes in the structure of the presynaptic neuron's axonal arborizations: When neighboring axons are destroyed, there is a shift of the remaining axonal arbors into deafferented regions and an increase in the number of putative contacts with the postsynaptic neuron. Changes in the structure of the presynaptic neuron also directly affect the probability of formation of this synaptic connection. The connection was found in 67% of the control specimens, but it was present in 100% of the partially deafferented specimens. The results demonstrate that interactions between growing sensory neurons can influence both the probability of synapse formation and the strength of those connections. This is the first case in which the effects of competition on the structure of a single, identified, presynaptic neuron can be directly related to its synaptic efficacy.Normal development of the nervous system requires not only that neurons make synaptic contact with the correct partners, but also that the strength of the synaptic input be adjusted to particular levels. One mechanism that is believed to regulate the number and efficacy of synaptic contacts is competition. The original idea, and much of the evidence for competitive interactions, come from studies of afferent projections in the visual system of vertebrates (Hubel et al., 1977;Schmidt et al., 1978;Tieman, 1984;Wiesel and Hubel, 1965). A direct demonstration, however, of the effects of competition on individual central synapses is difficult to obtain. The reason for this is numerical: In most vertebrate sensory systems there are large numbers of pre-and postsynaptic neurons, so one can never study the same synaptic connection under a variety of experimental conditions, and most studies have resorted to statistical sampling. In invertebrates, however, the numerical problems are reduced and it is possible to study identified central synapses physiologically. Here, we describe how competition influences the synaptic connection between an identified presynaptic neuron and an identified postsynaptic neuron in the CNS of the cricket. In brief, we demonstrate that synaptic efficacy, at a particular set of synaptic connections, is modulated by competition and that this is correlated with a change in the number of contacts made by the presynaptic neuron on the postsynaptic neuron.

Decreased monosynaptic sensory input to an identified motoneuron is associated with steroid-mediated dendritic regression during metamorphosis in Manduca sexta

“…A relationship between the number of synaptic contacts and the size of a synaptic response has been demonstrated in other systems (e.g., Kuno et al, 1971;Korn et al, 1981;Grantyn et al, 1984). A method commonly used to establish this relationship is quanta1 analysis of neurotransmitter release (Korn et al, 1982;Shepherd and Murphey, 1986;Hamon et al, 1990;Laurent and Sivaramakrishnan, 1992). Our working hypothesis predicts that binomial IZ, which is related to the number of synaptic contacts, would decrease during APR's regression.…”

“…Our working hypothesis predicts that binomial IZ, which is related to the number of synaptic contacts, would decrease during APR's regression. Similar information could potentially be gained by counting the number of synaptic contacts between individual PH afferents and APR using anatomical methods (e.g., Shepherd and Murphey, 1986;Blagburn and Thompson, 1990). Although our hypothesis relating the number of synaptic contacts to EPSP amplitude was formulated to account for developmental changes in EPSP amplitude, it may also account for the relationship between PH position and EPSP amplitude within a developmental stage (Figs.…”

Neural Mapping of Direction and Frequency in the Cricket Cercal Sensory System

“…Considerable evidence supports this latter possibility: afferents with different frequency-tuning properties have been demonstrated to make connections onto the same interneuron (Shepherd and Murphey, 1986;Chiba et al, 1988;Murphey 1993, 1994). Murphey (1993, 1994) suggested that a single afferent can connect to two different interneurons yet make synapses with very different properties: either habituating or facilitating.…”

Morphological plasticity of motor axons in Drosophila mutants with altered excitability

“…The invertebrate CNS has long been viewed as having a rigid stereotypic organization that precludes much plasticity (see Murphey, 1986). In recent years, however, studies of long-term physiological and anatomical changes in Aplysia during behav-ioral conditioning (Kandel et al, 1986;Bailey and Chen, 1988a,b), as well as studies of regeneration (Murphey and Lemere, 1984;Shepherd and Murphey, 1986;Loer et al, 1987;Loer and Kristan, 1989) have changed this view.…”

“…In recent years, however, studies of long-term physiological and anatomical changes in Aplysia during behav-ioral conditioning (Kandel et al, 1986;Bailey and Chen, 1988a,b), as well as studies of regeneration (Murphey and Lemere, 1984;Shepherd and Murphey, 1986;Loer et al, 1987;Loer and Kristan, 1989) have changed this view. Instead, it has become apparent that, even though the behavioral repertoire of invertebrates is less complex than that of vertebrates, developmental and physiological plasticity is a common feature (reviewed in Lnenicka and Murphey, 1989; see also Technau, 1984;Meinertzhagen, 1989).…”