Abstract
Intracellular recordings in GABAergic feedback neurons in the mushroom body of the honey bee brain revealed patterns of alternating neural activity. The recorded neurons have been identified via iontophoretic injection of Neurobiotin. The staining of groups of cells indicated dye coupling on the basis of gap junctions. The corresponding spike activity revealed spikes with different but overall comparatively low amplitudes (“spikelets”). The assumption of axo-axonal gap junctions would explain the staining of clusters of feedback neurons, alternating unit activity as well as spikelets with low amplitude. If a neuron in the electrically coupled network fires at a lower than maximal firing rate with respect to the refractory period, it will become more susceptible to laterally incoming spikes of neighbouring feedback neurons. In succession, the respective cell can be fully overtaken by neighbouring spike activity. On the one hand this proposed mechanism could lead to highly synchronous spike activity of a huge number of inhibitory synapses in the mushroom body calyces. On the other hand, the mechanism of laterally spreading activity could act like an amplifier. Additionally, the anatomical properties of Protocerebro Calycal Tract (PCT) feedback neurons could account for a reset function in order to allow for the changing activity profiles of the coupled cells. The laterally incoming potential would run in an antero- and retrograde direction. This could in principle lead to backpropagating inhibition of neighbouring PCT neurons and therefore a reset of one gating cycle. The proposed resulting oscillatory pattern of PCT activity has already been described in the literature and is confirmed by the physiological results, presented here.
Highlights
Synchrony of spike trains in the brain has a major function for the strengthening of synaptic contacts and the formation of phenomena such as long term potentiation (LTP)
Dye coupling of the recorded Protocerebro Calycal Tract (PCT) neurons occurred in every successful Neurobiotin injection (Figure 3A–F, for examples) except one anatomically exceptional PCT neuron, with no arborizations in the calycal region of the mushroom body neuropile (Figure 2)
Let us assume that neighbouring PCT neurons are firing at their maximal rate
Summary
Synchrony of spike trains in the brain has a major function for the strengthening of synaptic contacts and the formation of phenomena such as long term potentiation (LTP) (reviewed by Brown et al.[1]). Gap junction-mediated electrical coupling has been shown to be a potential source of synchrony and asynchrony[3]. Apart from mere synchrony effects, axoaxonal gap junctions in blowfly visual interneurons have been proposed to introduce a linear interpolation system between coupled neurons in order to visually extract the axis of rotation[4]. Gap junction-mediated quantum entanglement of microtubules has been proposed as a mechanism for very fast states of conscious perception[6]. The modality-specific topographic organization of Kenyon cells in the calycal regions is maintained throughout the mushroom body and causes a layered pattern of the lobes[11,13]. Feedback neurons are apparent in the mushroom bodies of a great variety of insect species (ant (Formica rufa, F. pratensis)[14], grasshopper (Acheta domesticus)[15,16], fly (Musca domestica)[17] and bees (Apis mellifera)[11,18])
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