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Abstract

To help elucidate the role of inhibitory feedback in the genesis of odour-evoked synchronization of neural activity, we investigated the distribution of gamma-aminobutyric acid (GABA)ergic synaptic terminals in the antennal lobes (AL) and mushroom bodies (MB) of the locust olfactory system. Electron-microscopy, intracellular horseradish peroxidase labelling, and immunocytochemistry were combined to assess the distribution of GABAergic synapses, using established methods (Leitch and Laurent [1993] J. Comp. Neurol. 337:461-470). In the AL, GABA-immunoreactive presynaptic terminals contacted both immunoreactive and immunonegative profiles. Conversely, GABA-immunoreactive profiles received direct input from both reactive and negative terminals. The tract containing the axons of the projection neurons that run from the AL to the MB contained about 830 axons of fairly uniform size, none of which was immunoreactive for GABA. In the calyx of the MB, large immunoreactive terminals contacted very-small-diameter profiles thought to belong to the Kenyon cells (KCs). This was confirmed by combining immunocytochemistry with intracellular HRP-labelling of KCs. KCs were not immunoreactive for GABA. Although some GABAergic contacts were made onto the spiny profiles of KCs, others were made onto their dendritic shafts. Large GABA-immunoreactive profiles were also found to contact large negative profiles that were presynaptic to KC terminals. This suggests that KC dendrites can be both pre- and post-synaptically inhibited in the calyx. The MB pedunculus contained ca. 50,000 tightly packed KC axons, showing conspicuous en passant and often reciprocal synaptic contacts between neighbouring axons. KC axons were immunonegative, but received direct input from, and contacted directly, large immunoreactive profiles running across or along the KC axons. In the alpha- and beta-lobes of the MB, connections similar to those in the pedunculus were seen with two main differences: (1) The density of synaptic profiles was higher, giving on occasion numerous serially connected profiles in a single section; (2) large immunonegative profiles with dense-core vesicles were abundant and were frequently presynaptic to GABAergic processes and to very-small-diameter profiles which possibly belong to KCs. These results are discussed in the context of the known physiological data on olfactory processing in these complex circuits.