Neural plasticity of mushroom body-extrinsic neurons in the honeybee brain

Menzel, Randolf; Manz, Gisela

doi:10.1242/jeb.01908

Cited by 78 publications

(54 citation statements)

References 68 publications

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“…As shown in mammals, long-term potentiation or depression may recruit differential molecular mechanisms, such as NMDA receptor activation 32,33 and retrograde signalling by endocannabinoids [32][33][34] . Such depression may occur in the MB-efferent synapses during memory acquisition 35 , although underlying mechanisms are still yet to be identified in Drosophila. Interestingly, in Drosophila, the GABAergic APL neuron that projects onto the MB shows a reduced response to the trained odour 36 .…”

Section: Discussionmentioning

confidence: 99%

Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila

Séjourné¹,

Plaçais²,

et al. 2011

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6 These authors contributed equally to this work. 2 Aversive olfactory memory is formed in the Drosophila mushroom bodies (MB).Memory retrieval requires MB output, but it remains unknown how a memory trace in the MB drives conditioned avoidance of a learned odour. To identify neurons involved in olfactory memory retrieval, we performed an anatomical and functional screen of defined sets of MB extrinsic neurons. Here we show that MB-V2 neurons are essential for retrieval of both short-and long-lasting memory, but neither for memory formation nor for memory consolidation. We further show that MB-V2 are cholinergic efferent neurons that project from the MB vertical lobes to the middle superiormedial protocerebrum and the lateral horn (LH). Notably, the odour response of MB-V2 neurons is modified after conditioning. As the LH is implicated in innate responses to repellent odorants, we propose that during memory retrieval, MB-V2 neurons reinforce the olfactory pathway involved in innate odour avoidance.Different odours induce innate approach or avoidance behaviours in Drosophila. Innate odour responses can be modulated by experience, such as associative learning. After simultaneous exposure to an electric shock and an odorant, flies form aversive memory and show robust conditioned odour avoidance that lasts for hours to days, depending on the training protocol [1][2][3] . The neural pathways for odour or shock processing and signal integration in the fly brain have been intensely studied in recent years. Odour information is first represented in the antennal lobes in the form of olfactory receptor neuron activity 4 . Projection neurons then convey this information to higher order processing centres 4 : the mushroom bodies (MB) and the lateral horn (LH). In contrast, aversive reinforcement signals in response to electric shock are relayed to the MB via dopaminergic neurons [5][6][7] . The olfactory and 3 electric shock signals are integrated in the MB to form aversive olfactory memory 1, 2 . The MB are however dispensable for innate avoidance of the repellent odours 8,9 .In adult Drosophila, the MB consist of approximately 2000 Kenyon cells per brain hemisphere, which may be classified into three major types based on their axonal projection: γ neurons, which form only a medial lobe, α/β neurons, whose axons branch to form a vertical (α) and a medial (β) lobe, and α'/β' neurons, which also form a vertical (α') and a medial (β') lobe 10 . Functional brain imaging has revealed localised activation of cAMP/PKA signalling in the MB α lobe in response to simultaneous cholinergic and dopaminergic stimulation 11,12 , that represent respectively the odorant and electric shock pathways.Following associative conditioning, calcium imaging studies have shown that a short-term memory trace is formed in the α'/β' neurons 13, and a long-term one in α lobes 14 . Previous studies have shown that the output of the α/β neurons is necessary for the retrieval of all phases of olfactory memory 15,16 , but the neural circuits that translate ...

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Section: Discussionmentioning

confidence: 99%

Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila

Séjourné¹,

Plaçais²,

et al. 2011

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“…It is thus less likely that they are selectively tuned to particular stimulus combinations; rather, they may reflect the history of experience with the stimuli. Evidence for this view comes from recordings from an identified EN in this region, the PE1 neuron, which was found to respond to a large range of stimuli (olfactory, mechanosensory, visual), and changes its response profile as a consequence of olfactory learning (Mauelshagen, 1993;Menzel and Manz, 2005;Okada et al, 2007). Here we focused on other ENs.…”

Section: Discussionmentioning

confidence: 99%

Mushroom Body Output Neurons Encode Odor–Reward Associations

Strube-Bloss¹,

Nawrot²,

Menzel³

2011

J. Neurosci.

142

175

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Neural correlates of learning and memory formation have been reported at different stages of the olfactory pathway in both vertebrates and invertebrates. However, the contribution of different neurons to the formation of a memory trace is little understood. Mushroom bodies (MBs) in the insect brain are higher-order structures involved in integration of olfactory, visual, and mechanosensory information and in memory formation. Here we focus on the ensemble spiking activity of single MB output neurons (ENs) when honeybees learned to associate an odor with reward. A large group of ENs (ϳ50%) changed their odor response spectra by losing or gaining sensitivity for specific odors. This response switching was dominated by the rewarded stimulus (CSϩ), which evoked exclusively recruitment. The remaining ENs did not change their qualitative odor spectrum but modulated their tuning strength, again dominated by increased responses to the CSϩ. While the bees showed a conditioned response (proboscis extension) after a few acquisition trials, no short-term effects were observed in the neuronal activity. In both EN types, associative plastic changes occurred only during retention 3 h after conditioning. Thus, long-term but not short-term memory was reflected by increased EN activity to the CSϩ. During retention, the EN ensemble separated the CSϩ most differently from the CSϪ and control odors ϳ140 ms after stimulus onset. The learned behavioral response appeared ϳ330 ms later. It is concluded that after memory consolidation, the ensemble activity of the MB output neurons predicts the meaning of the stimulus (reward) and may provide the prerequisite for the expression of the learned behavior.

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“…Mushroom body neurons exhibit spike-timing-dependent plasticity (Mauelshagen, 1993;Li and Strausfeld, 1997;Menzel and Manz, 2005;Cassenaer and Laurent, 2007). The precise spiking characteristics of the layer 5-6 neurons could be essential for inducing these spike-timing-dependent changes in the mushroom body and protocerebral neurons.…”

Section: Lobula Output Regions Indicate Behavioral Relevancementioning

confidence: 99%

The Processing of Color, Motion, and Stimulus Timing Are Anatomically Segregated in the Bumblebee Brain

Paulk

Phillips-Portillo

Dacks

et al. 2008

Journal of Neuroscience

119

161

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Animals use vision to perform such diverse behaviors as finding food, interacting socially with other animals, choosing a mate, and avoiding predators. These behaviors are complex and the visual system must process color, motion, and pattern cues efficiently so that animals can respond to relevant stimuli. The visual system achieves this by dividing visual information into separate pathways, but to what extent are these parallel streams separated in the brain? To answer this question, we recorded intracellularly in vivo from 105 morphologically identified neurons in the lobula, a major visual processing structure of bumblebees (Bombus impatiens). We found that these cells have anatomically segregated dendritic inputs confined to one or two of six lobula layers. Lobula neurons exhibit physiological characteristics common to their respective input layer. Cells with arborizations in layers 1-4 are generally indifferent to color but sensitive to motion, whereas layer 5-6 neurons often respond to both color and motion cues. Furthermore, the temporal characteristics of these responses differ systematically with dendritic branching pattern. Some layers are more temporally precise, whereas others are less precise but more reliable across trials. Because different layers send projections to different regions of the central brain, we hypothesize that the anatomical layers of the lobula are the structural basis for the segregation of visual information into color, motion, and stimulus timing.

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Neural plasticity of mushroom body-extrinsic neurons in the honeybee brain

Cited by 78 publications

References 68 publications

Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila

Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila

Mushroom Body Output Neurons Encode Odor–Reward Associations

The Processing of Color, Motion, and Stimulus Timing Are Anatomically Segregated in the Bumblebee Brain

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