Short Neuropeptide F Acts as a Functional Neuromodulator for Olfactory Memory in Kenyon Cells of Drosophila Mushroom Bodies

In order to represent complex stimuli, principle neurons of associative learning regions receive combinatorial sensory inputs. Density of combinatorial innervation is theorized to determine the number of distinct stimuli that can be represented and distinguished from one another, with sparse innervation thought to optimize the complexity of representations in networks of limited size. How the convergence of combinatorial inputs to principle neurons of associative brain regions is established during development is unknown. Here, we explore the developmental patterning of sparse olfactory inputs to Kenyon cells of the Drosophila melanogaster mushroom body. By manipulating the ratio between pre- and post-synaptic cells, we find that postsynaptic Kenyon cells set convergence ratio: Kenyon cells produce fixed distributions of dendritic claws while presynaptic processes are plastic. Moreover, we show that sparse odor responses are preserved in mushroom bodies with reduced cellular repertoires, suggesting that developmental specification of convergence ratio allows functional robustness.

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Nitric oxide augments single persistent Na+ channel currents via the cGMP/PKG signaling pathway in Kenyon cells isolated from cricket mushroom bodies

Journal of Neurophysiology ◽

10.1152/jn.00440.2017 ◽

2018 ◽

Vol 120 (2) ◽

pp. 720-728 ◽

Cited By ~ 1

Author(s):

Mariko Ikeda ◽

Masami Yoshino

Keyword(s):

Nitric Oxide ◽

Signaling Pathway ◽

Single Channel ◽

Signaling Cascade ◽

Mushroom Bodies ◽

Na Channel ◽

No Production ◽

Kenyon Cells ◽

Single Channel Currents ◽

Channel Currents

The nitric oxide (NO)/cyclic GMP signaling pathway has been suggested to be important in the formation of olfactory memory in insects. However, the molecular targets of the NO signaling cascade in the central neurons associated with olfactory learning and memory have not been fully analyzed. In this study, we investigated the effects of NO donors on single voltage-dependent Na+ channels in intrinsic neurons, called Kenyon cells, in the mushroom bodies in the brain of the cricket. Step depolarization on cell-attached patch membranes induces single-channel currents with fast-activating and -inactivating brief openings at the beginning of the voltage steps followed by more persistently recurring brief openings all along the 150-ms pulses. Application of the NO donor S-nitrosoglutathione (GSNO) increased the number of channel openings of both types of single Na+ channels. This excitatory effect of GSNO on the activity of these Na+ channels was diminished by KT5823, an inhibitor of protein kinase G (PKG), indicating an involvement of PKG in the downstream pathway of NO. Application of KT5823 alone decreased the activity of the persistent Na+ channels without significant effects on the fast-inactivating Na+ channels. The membrane-permeable cGMP analog 8Br-cGMP increased the number of channel openings of both types of single Na+ channels, similar to the action of NO. Taken together, these results indicate that NO acts as a critical modulator of both fast-inactivating and persistent Na+ channels and that persistent Na+ channels are constantly upregulated by the endogenous cGMP/PKG signaling cascade. NEW & NOTEWORTHY This study clarified that nitric oxide (NO) increases the activity of both fast-inactivating and persistent Na+ channels via the cGMP/PKG signaling cascade in cricket Kenyon cells. The persistent Na+ channels are also found to be upregulated constantly by endogenous cGMP/PKG signaling. On the basis of the present results and the results of previous studies, we propose a hypothetical model explaining NO production and NO-dependent memory formation in cricket large Kenyon cells.

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The brain of the honeybee Apis mellifera . I. The connections and spatial organization of the mushroom bodies

Philosophical Transactions of the Royal Society of London Series B Biological Sciences ◽

10.1098/rstb.1982.0086 ◽

1982 ◽

Vol 298 (1091) ◽

pp. 309-354 ◽

Cited By ~ 347

Keyword(s):

Visual Information ◽

Spatial Organization ◽

Short Term Memory ◽

Single Layer ◽

Mushroom Bodies ◽

After Effects ◽

Kenyon Cells ◽

The Individual ◽

Polar Organization ◽

The Brain

The mushroom bodies of the bee are paired neuropils in the dorsal part of the brain. Each is composed of the arborizations of over 17 x 10 4 small interneurons of similar architecture called Kenyon cells. Golgi staining demonstrates that these neurons can be divided into five groups distinguished on the basis of their dendritic specializations and geometry. The mushroom body neuropils each consist of a pair of cup-shaped structures, the calyces, connected by two short fused stalks, the pedunculus, to two lobes, the α- and β-lobes. Each calyx is formed from three concentric neuropil zones, the basal ring, the collar and the lip. The calyces are organized in a polar fashion; within the calyces each of the five categories of Kenyon cell has a distribution limited to particular polar contours. The dendritic volumes of neighbouring Kenyon cells arborizing within each individual contour are greatly overlapped. Fibres from groups of neighbouring cells within a calycal contour are gathered into bundles that project into the pedunculus, each fibre dividing to enter both the the α- and β-lobes. The pedunculus and the lobes are conspicuously layered. Kenyon cells with neighbouring dendritic fields within the same calycal contour occupy a single layer in the pedunculus and lobes. Thus the two- polar organization of the calyces is transformed into a Cartesian map within the pedunculus, which continues into the α- and β-lobes. The calyx receives input fibres from both the antennal lobes and the optic neuropils. The branching patterns of these cells reflect the polar organization of the calyces as their terminals are restricted to one or more of the three gross compartments of the calycal neuropil. The course of these tracts and the morphologies of the fibres that they contain are described. Cells considered to represent outputs from the mushroom bodies arborize in the pedunculus and α- and β-lobes. Generally the arborizations of the output neurons reflect the layered organization of these neuropils. Fibres from the two lobes run to the anterior median and lateral protocerebral neuropil, and the anterior optic tubercle. Additionally there is an extensive network of feedback interneurons that inter- connect the α- and β-lobes with the ipsi- and contralateral calyces. Many individual neurons have branches in both the α- and β-lobes and in the pedunculus. The pathways and geometries of the fibres subserving the two lobes are described. The hypothesis of Vowles (1955) that the individual lobes represent a separation of sensory and motor output areas is shown to be incorrect. The anatomy of the bee’s mushroom bodies suggests that they process second-order antennal and fourth- and higher-order visual information. The feedback pathways are discussed as possible means of creating long-lasting after-effects which may be important in complex timing processes and possibly the formation of short-term memory.

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Nicotinic acetylcholine currents of cultured Kenyon cells from the mushroom bodies of the honey beeApis mellifera

The Journal of Physiology ◽

10.1111/j.1469-7793.1999.759ad.x ◽

1999 ◽

Vol 514 (3) ◽

pp. 759-768 ◽

Cited By ~ 75

Author(s):

Frank Goldberg ◽

Bernd Grünewald ◽

Hendrik Rosenboom ◽

Randolf Menzel

Keyword(s):

Mushroom Bodies ◽

Nicotinic Acetylcholine ◽

Kenyon Cells

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Drosophila Mushroom Body Kenyon Cells Generate Spontaneous Calcium Transients Mediated by PLTX-Sensitive Calcium Channels

Journal of Neurophysiology ◽

10.1152/jn.00096.2005 ◽

2005 ◽

Vol 94 (1) ◽

pp. 491-500 ◽

Cited By ~ 30

Author(s):

Shaojuan Amy Jiang ◽

Jorge M. Campusano ◽

Hailing Su ◽

Diane K. O'Dowd

Keyword(s):

Calcium Channels ◽

Late Stage ◽

Calcium Oscillations ◽

Adult Brain ◽

Calcium Transients ◽

Mushroom Bodies ◽

Brain Neurons ◽

Voltage Gated ◽

Voltage Gated Calcium Channels ◽

Kenyon Cells

Spontaneous calcium oscillations in mushroom bodies of late stage pupal and adult Drosophila brains have been implicated in memory consolidation during olfactory associative learning. This study explores the cellular mechanisms regulating calcium dynamics in Kenyon cells, principal neurons in mushroom bodies. Fura-2 imaging shows that Kenyon cells cultured from late stage Drosophila pupae generate spontaneous calcium transients in a cell autonomous fashion, at a frequency similar to calcium oscillations in vivo (10–20/h). The expression of calcium transients is up regulated during pupal development. Although the ability to generate transients is a property intrinsic to Kenyon cells, transients can be modulated by bath application of nicotine and GABA. Calcium transients are blocked, and baseline calcium levels reduced, by removal of external calcium, addition of cobalt, or addition of Plectreurys toxin (PLTX), an insect-specific calcium channel antagonist. Transients do not require calcium release from intracellular stores. Whole cell recordings reveal that the majority of voltage-gated calcium channels in Kenyon cells are PLTX-sensitive. Together these data show that influx of calcium through PLTX-sensitive voltage-gated calcium channels mediates spontaneous calcium transients and regulates basal calcium levels in cultured Kenyon cells. The data also suggest that these calcium transients represent cellular events underlying calcium oscillations in the intact mushroom bodies. However, spontaneous calcium transients are not unique to Kenyon cells as they are present in approximately 60% of all cultured central brain neurons. This suggests the calcium transients play a more general role in maturation or function of adult brain neurons.

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Lipophorin receptors regulate mushroom bodies development and participate in learning, memory, and sleep in flies

10.1101/2021.11.10.467940 ◽

2021 ◽

Author(s):

Francisca Rojo-Cortes ◽

Victoria Tapia-Valladares ◽

Nicolas Fuenzalida-Uribe ◽

Sergio Hidalgo ◽

Candy B. Roa ◽

...

Keyword(s):

Adaptor Protein ◽

Mammalian Brain ◽

Mushroom Bodies ◽

Lipid Uptake ◽

Olfactory Memory ◽

Drosophila Brain ◽

Association Area ◽

Reelin Signaling ◽

And Function

Drosophila melanogaster Lipophorin Receptors, LpR1 and LpR2, mediate lipid uptake. The orthologs of these receptors in vertebrates, ApoER2 and VLDL-R, bind Reelin, a glycoprotein not present in flies. These receptors are associated with the development and function of the hippocampus and cerebral cortex, important association areas in the mammalian brain. It is currently unknown whether LpRs play similar roles in the Drosophila brain. We report that LpR-deficient flies exhibit impaired olfactory memory and sleep patterns, which seem to reflect anatomical defects found in a critical brain association area, the Mushroom Bodies (MB). Moreover, cultured MB neurons respond to mammalian Reelin by increasing the complexity of their neurites. This effect depends on LpRs and Dab, the Drosophila ortholog of the reelin signaling adaptor protein Dab1. In vitro, two of the long isoforms of LpRs allow the internalization of Reelin. Overall, these findings demonstrate that LpRs contribute to MB development and function, supporting the existence of LpR-dependent signaling in Drosophila.

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Modular subdivision of mushroom bodies by kenyon cells in the silkmoth

The Journal of Comparative Neurology ◽

10.1002/cne.21946 ◽

2009 ◽

Vol 513 (3) ◽

pp. 315-330 ◽

Cited By ~ 17

Author(s):

Ryota Fukushima ◽

Ryohei Kanzaki

Keyword(s):

Mushroom Bodies ◽

Kenyon Cells

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Drosophila mushroom bodies integrate hunger and satiety signals to control innate food-seeking behavior

eLife ◽

10.7554/elife.35264 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 49

Author(s):

Chang-Hui Tsao ◽

Chien-Chun Chen ◽

Chen-Han Lin ◽

Hao-Yu Yang ◽

Suewei Lin

Keyword(s):

Dopaminergic Neurons ◽

Mushroom Body ◽

Energy State ◽

Fruit Fly ◽

Mushroom Bodies ◽

Kenyon Cells ◽

Control Food ◽

Seeking Behavior ◽

Output Neurons ◽

Food Seeking

The fruit fly can evaluate its energy state and decide whether to pursue food-related cues. Here, we reveal that the mushroom body (MB) integrates hunger and satiety signals to control food-seeking behavior. We have discovered five pathways in the MB essential for hungry flies to locate and approach food. Blocking the MB-intrinsic Kenyon cells (KCs) and the MB output neurons (MBONs) in these pathways impairs food-seeking behavior. Starvation bi-directionally modulates MBON responses to a food odor, suggesting that hunger and satiety controls occur at the KC-to-MBON synapses. These controls are mediated by six types of dopaminergic neurons (DANs). By manipulating these DANs, we could inhibit food-seeking behavior in hungry flies or promote food seeking in fed flies. Finally, we show that the DANs potentially receive multiple inputs of hunger and satiety signals. This work demonstrates an information-rich central circuit in the fly brain that controls hunger-driven food-seeking behavior.

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