Abstract
In the insect brain, the mushroom body is a higher order brain area that is key to memory formation and sensory processing. Mushroom body (MB) extrinsic neurons leaving the output region of the MB, the lobes and the peduncle, are thought to be especially important in these processes. In the honeybee brain, a distinct class of MB extrinsic neurons, A3 neurons, are implicated in playing a role in learning. Their MB arborisations are either restricted to the lobes and the peduncle, here called A3 lobe connecting neurons, or they provide feedback information from the lobes to the input region of the MB, the calyces, here called A3 feedback neurons. In this study, we analyzed the morphology of individual A3 lobe connecting and feedback neurons using confocal imaging. A3 feedback neurons were previously assumed to innervate each lip compartment homogenously. We demonstrate here that A3 feedback neurons do not innervate whole subcompartments, but rather innervate zones of varying sizes in the MB lip, collar, and basal ring. We describe for the first time the anatomical details of A3 lobe connecting neurons and show that their connection pattern in the lobes resemble those of A3 feedback cells. Previous studies showed that A3 feedback neurons mostly connect zones of the vertical lobe that receive input from Kenyon cells of distinct calycal subcompartments with the corresponding subcompartments of the calyces. We can show that this also applies to the neck of the peduncle and the medial lobe, where both types of A3 neurons arborize only in corresponding zones in the calycal subcompartments. Some A3 lobe connecting neurons however connect multiple vertical lobe areas. Contrarily, in the medial lobe, the A3 neurons only innervate one division. We found evidence for both input and output areas in the vertical lobe. Thus, A3 neurons are more diverse than previously thought. The understanding of their detailed anatomy might enable us to derive circuit models for learning and memory and test physiological data.
Highlights
The mushroom body (MB) in the insect brain is key to memory formation and sensory processing (Heisenberg, 2003; Menzel, 2014; Aso and Rubin, 2016)
We evaluated the morphology of 31 A3 neurons including nine single stained cells (n = 15 animals)
The name feedback neurons is adapted from previous studies and refers to this group feeding back information from the mushroombody output area to the mushroombody input area (Gronenberg, 1987; Rybak and Menzel, 1993; Grünewald, 1999b)
Summary
The mushroom body (MB) in the insect brain is key to memory formation and sensory processing (Heisenberg, 2003; Menzel, 2014; Aso and Rubin, 2016). KC are arranged in such a way that each calycal subcompartment is presented in a separated layer in the vertical lobe, the peduncle, and the medial lobe (Mobbs, 1982; Rybak and Menzel, 1993; Strausfeld, 2002). In these lobes KCs connect to a variety of MB extrinsic neurons including a group of about 110 GABAergic neurons called A3 neurons (Bicker et al, 1988; Rybak and Menzel, 1993). Inhibitory feedback neurons are found in locusts (Leitch and Laurent, 1996; Papadopoulou et al, 2011) and cockroaches (Weiss, 1974; Nishino and Mizunami, 1998; Yamazaki et al, 1998; Strausfeld and Li, 1999; Takahashi et al, 2017)
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