Anatomical plasticity of synapses in the lamina of the optic lobe of the fly

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Abstract
Insects are frequently assumed to have hard-wired nervous systems that fail to demonstrate functional plasticity. We have produced changes in synaptic frequency, and analysed their developmental time course, dynamics and reversibility, in the lamina underlying the compound eye of the fly, by exposing young adults to different visual stimuli. The class of synapse examined feeds back from L2, one of the monopolar cells found in each lamina cartridge, to photoreceptor terminals; each site is a synaptic dyad marked by the presence of a few, round vesicles surrounding a T - shaped presynaptic ribbon and, in the photoreceptor, by a subsynaptic vacuole. In control adult flies reared in normal room lighting, the frequency of synaptic profiles scored in micrographs of single sections initially increased until one day post-eclosion (E+l), but declined thereafter. Frequencies measured in left and right eyes of the same control animals were closely matched. Experimental flies were put for one to two days into an integrating sphere illuminated continuously with square-wave, 25 Hz green light. They had one eye occluded, so providing control comparisons between flicker-reared (FR) and occluded (dark-reared,DR) eyes within the same animal. TheDReyes invariably (n> 22) had higher frequencies of synaptic profiles than those seeing light, regardless of age or the period of light exposure, although the detailed relative effects ofFRandDRdepend upon the age of the animal. The evidence suggests that exposure to light actively depresses synaptic frequency and increases its variability. The greatest difference (30%) achieved was at two to four days after eclosion and there was no difference beyond six days, so demarcating a prospective sensitive period. Rearing in dc light was equally effective as FRso visual contrastsper seare apparently inessential. Frequency values can change rapidly. During the first 24 h post-eclosion, dr resulted in new synapses adding to L2’s complement of 25-35 at a maximum rate of 4 per 6 h, whereas light exposure caused a frequency decrease after as little as 6 h. Alternating 24 h periods of light and dark during the first two days produced reversible synaptic frequency changes. Individual synaptic contacts enlarge with age but not significantly with different visual experiences. The decrease in frequency of synaptic profiles with age thus actually underestimates the true decrease in synaptic number, whereas the altered synaptic frequencies seen after differential exposure represent true differences in synaptic number. The length of the axon of L2 is fixed, but its diameter increases, both with age andDR, although neither change generates the altered frequencies. Thus the L2 feedback synapse is plastic during the first four days of adult life, a conclusion validated by definitive counts of synaptic sites in short micrograph series. We cannot exclude, however, that the observed changes in the number of sampled synapses reflect individual synaptic contacts within a fixed population breaking and re-forming, so as to change their proximo-distal distribution.