Neural Organization of A3 Mushroom Body Extrinsic Neurons in the Honeybee Brain

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...

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Main Authors: Hanna Zwaka, Ruth Bartels, Bernd Grünewald, Randolf Menzel
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-08-01
Series:Frontiers in Neuroanatomy
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnana.2018.00057/full
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author Hanna Zwaka
Hanna Zwaka
Ruth Bartels
Bernd Grünewald
Randolf Menzel
Randolf Menzel
author_facet Hanna Zwaka
Hanna Zwaka
Ruth Bartels
Bernd Grünewald
Randolf Menzel
Randolf Menzel
author_sort Hanna Zwaka
collection DOAJ
description 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.
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spelling doaj.art-d227199028234290b5941f49db9270c12022-12-21T20:09:15ZengFrontiers Media S.A.Frontiers in Neuroanatomy1662-51292018-08-011210.3389/fnana.2018.00057350769Neural Organization of A3 Mushroom Body Extrinsic Neurons in the Honeybee BrainHanna Zwaka0Hanna Zwaka1Ruth Bartels2Bernd Grünewald3Randolf Menzel4Randolf Menzel5Institute of Neurobiology, Free University Berlin, Berlin, GermanyMolecular and Cellular Biology, Harvard University, Cambridge, MA, United StatesInstitute of Neurobiology, Free University Berlin, Berlin, GermanyInstitut für Bienenkunde Oberursel, Goethe University Frankfurt, Frankfurt, GermanyInstitute of Neurobiology, Free University Berlin, Berlin, GermanyBernstein Center for Computational Neuroscience, Berlin, GermanyIn 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.https://www.frontiersin.org/article/10.3389/fnana.2018.00057/fullGABAhoneybeemushroom bodiesmemoryfeedback neuronsmushroom body extrinsic neurons
spellingShingle Hanna Zwaka
Hanna Zwaka
Ruth Bartels
Bernd Grünewald
Randolf Menzel
Randolf Menzel
Neural Organization of A3 Mushroom Body Extrinsic Neurons in the Honeybee Brain
Frontiers in Neuroanatomy
GABA
honeybee
mushroom bodies
memory
feedback neurons
mushroom body extrinsic neurons
title Neural Organization of A3 Mushroom Body Extrinsic Neurons in the Honeybee Brain
title_full Neural Organization of A3 Mushroom Body Extrinsic Neurons in the Honeybee Brain
title_fullStr Neural Organization of A3 Mushroom Body Extrinsic Neurons in the Honeybee Brain
title_full_unstemmed Neural Organization of A3 Mushroom Body Extrinsic Neurons in the Honeybee Brain
title_short Neural Organization of A3 Mushroom Body Extrinsic Neurons in the Honeybee Brain
title_sort neural organization of a3 mushroom body extrinsic neurons in the honeybee brain
topic GABA
honeybee
mushroom bodies
memory
feedback neurons
mushroom body extrinsic neurons
url https://www.frontiersin.org/article/10.3389/fnana.2018.00057/full
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