Abstract

Gap junctions are widely distributed in the brains across species and play essential roles in neural information processing. However, the role of gap junctions in insect cognition remains poorly understood. Using a flight simulator paradigm and genetic tools, we found that gap junctions are present in Drosophila Kenyon cells (KCs), the major neurons of the mushroom bodies (MBs), and showed that they play an important role in visual learning and memory. Using a dye coupling approach, we determined the distribution of gap junctions in KCs. Furthermore, we identified a single pair of MB output neurons (MBONs) that possess a gap junction connection to KCs, and provide strong evidence that this connection is also required for visual learning and memory. Together, our results reveal gap junction networks in KCs and the KC-MBON circuit, and bring new insight into the synaptic network underlying fly's visual learning and memory.

Highlights

  • In addition to chemical synapses, neurons communicate via gap junctions, called electrical synapses

  • We found that visual learning and memory was impaired when a/b neurons of Kenyon cells (KCs), driven by 17d-GAL4, were hyperpolarized, and the memory was restored when GAL4 activity was blocked in mushroom bodies (MBs) by MB247-GAL80 (Figure 1B, upper panel)

  • Hyperpolarizing a’/b’ neurons with MB370B-GAL4, g neurons with MB131B-GAL4, or a/b and g neurons of KCs with MB247GAL4 abolished visual learning and memory (Figure 1B lower panel). These results indicate that KCs participate in visual learning and memory

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Summary

Introduction

In addition to chemical synapses, neurons communicate via gap junctions, called electrical synapses. A gap junction consists of an intercellular channel that is formed by two hemichannels, each containing six homo- or heteromeric protein subunits. These subunits belong to the connexin or pannexin gene families in vertebrates and the innexin (inx) gene family in invertebrates. The synchronization of neurons through the function of gap junctions was proposed to play a key role in cognitive processes, such as perception, attention, as well as learning and memory (Bissiere et al, 2011; Hormuzdi et al, 2004; Tamas et al, 2000). Insects have much simpler neural systems, yet still perform sophisticated cognitive functions, the role of gap junctions in cognition has rarely been investigated

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