Mushroom body output differentiates memory processes and distinct memory-guided behaviors

Ichinose, Toshiharu; Kanno, Mai; Wu, Hongyang; Yamagata, Nobuhiro; Sun, Huan; Abe, Ayako; Tanimoto, Hiromu

doi:10.1016/j.cub.2020.12.032

Cited by 14 publications

(12 citation statements)

References 75 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This suggests that redundancy and/or different weighting across approach promoting MBONs renders the system resilient to silencing some of them. A previous study found effects of blocking the γ2α′1 MBONs, though not γ3/γ3β′1 MBONs, when blocking individual steps of memory processing (acquisition, retention, and/or retrieval) with a 1 hr appetitive memory protocol ( Ichinose et al, 2021 ). This suggests that the different MBONs have differing roles across time, with some redundancy in appetitive processing.…”

Section: Discussionmentioning

confidence: 95%

“…In addition, reciprocal connections between KCs and dopaminergic neurons in the vertical lobes are necessary for memory retrieval ( Cervantes-Sandoval et al, 2017 ). This adds another layer of recurrent circuitry that may participate in reinforcement during associative learning ( Aso et al, 2014b ; Ichinose et al, 2015 ; Ichinose et al, 2021 ). Across these circuits, some neurons corelease several neurotransmitters and act on an array of postsynaptic receptors, which contribute to plasticity distributed across multiple sites ( Aso et al, 2019 ; Barnstedt et al, 2016 ; Berry et al, 2012 ; Bielopolski et al, 2019 ; Cohn et al, 2015 ; Handler et al, 2019 ; Haynes et al, 2015 ; Keene et al, 2004 ; Kim et al, 2007 ; Liu and Davis, 2009 ; Pribbenow et al, 2021 ; Schroll et al, 2006 ; Séjourné et al, 2011 ; Silva et al, 2015 ; Wu et al, 2013 ; Zhou et al, 2019 ).…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Associative learning drives longitudinally graded presynaptic plasticity of neurotransmitter release along axonal compartments

Stahl

Noyes

Boto

et al. 2022

eLife

View full text Add to dashboard Cite

Anatomical and physiological compartmentalization of neurons is a mechanism to increase the computational capacity of a circuit, and a major question is what role axonal compartmentalization plays. Axonal compartmentalization may enable localized, presynaptic plasticity to alter neuronal output in a flexible, experience-dependent manner. Here we show that olfactory learning generates compartmentalized, bidirectional plasticity of acetylcholine release that varies across the longitudinal compartments of Drosophila mushroom body (MB) axons. The directionality of the learning-induced plasticity depends on the valence of the learning event (aversive vs. appetitive), varies linearly across proximal to distal compartments following appetitive conditioning, and correlates with learning-induced changes in downstream mushroom body output neurons (MBONs) that modulate behavioral action selection. Potentiation of acetylcholine release was dependent on the CaV2.1 calcium channel subunit cacophony. In addition, contrast between the positive conditioned stimulus and other odors required the inositol triphosphate receptor (IP3R), which maintained responsivity to odors upon repeated presentations, preventing adaptation. Downstream from the mushroom body, a set of MBONs that receive their input from the g3 MB compartment were required for normal appetitive learning, suggesting that they represent a key node through which reward learning influences decision-making. These data demonstrate that learning drives valence-correlated, compartmentalized, bidirectional potentiation and depression of synaptic neurotransmitter release, which rely on distinct mechanisms and are distributed across axonal compartments in a learning circuit.

show abstract

Section: Discussionmentioning

confidence: 95%

Section: Discussionmentioning

confidence: 99%

Associative learning drives longitudinally graded presynaptic plasticity of neurotransmitter release along axonal compartments

Stahl

Noyes

Boto

et al. 2022

eLife

View full text Add to dashboard Cite

show abstract

“…Finally, we asked if UpWiNs are required for retrieval of sugar-induced appetitive memory. Formation of long-lasting appetitive memory after odor-sugar conditioning relies on the DANs that innervate the α1 compartment (Ichinose et al, 2021; Yamagata et al, 2015). Therefore, we tested the requirement of UpWiNs for 1-day appetitive memory.…”

Section: Resultsmentioning

confidence: 99%

“…For example, memory formation in the α1 compartment requires relatively long training, but once formed, lasts more than a day. In contrast, memory in γ5β’2a requires only a single training to form but is transient and easily overwritten by the subsequent training (Aso and Rubin, 2016; Ichinose et al, 2021; Yamada et al, n.d.). Compartments are also tuned to distinct types of reward.…”

Section: Introductionmentioning

confidence: 99%

Neural circuit mechanisms for transforming learned olfactory valences into wind-oriented movement

Aso

Yamada

Bushey

et al. 2022

Preprint

View full text Add to dashboard Cite

How memories are used by the brain to guide future action is poorly understood. In olfactory associative learning in Drosophila, multiple compartments of the mushroom body act in parallel to assign valence to a stimulus. Here, we show that appetitive memories stored in different compartments induce different levels of upwind locomotion. Using a photoactivation screen of a new collection of split-GAL4 drivers and EM connectomics, we identified a cluster of neurons postsynaptic to the mushroom body output neurons (MBONs) that can trigger robust upwind steering. These UpWind Neurons (UpWiNs) integrate inhibitory and excitatory synaptic inputs from MBONs of appetitive and aversive memory compartments, respectively. After training, disinhibition from the appetitive-memory MBONs enhances the response of UpWiNs to reward-predicting odors. Blocking UpWiNs impaired appetitive memory and reduced upwind locomotion during retrieval. Photoactivation of UpWiNs also increased the chance of returning to a location where activation was initiated, suggesting an additional role in olfactory navigation. Thus, our results provide insight into how learned abstract valences are gradually transformed into concrete memory-driven actions through divergent and convergent networks, a neuronal architecture that is commonly found in the vertebrate and invertebrate brains.

show abstract

“…4 D)—contributing to movement suppression, which is further supported by our unpublished study demonstrating that ectopic inhibition of MBON-γ2α’1 via Shi ts leads to loss of inhibitory control. MBON-γ2α’1 activity is shown to be crucial for various aspects of appetitive and aversive memory 31 , 56 – 60 , courtship memory 61 , sleep promotion 31 , 62 , 63 , fat accumulation 64 , food seeking 65 and attraction/positive valence 31 . Regarding stimulus-induced motor behaviors, ectopic activation of MBON-γ2α’1 causes inhibition of proboscis extension response to sucrose but ectopic inhibition has no effect 66 .…”

Section: Discussionmentioning

confidence: 99%

Acetylcholine deficit causes dysfunctional inhibitory control in an aging-dependent manner

Sabandal

Saldes

Han

2022

Sci Rep

View full text Add to dashboard Cite

Inhibitory control is a key executive function that limits unnecessary thoughts and actions, enabling an organism to appropriately execute goal-driven behaviors. The efficiency of this inhibitory capacity declines with normal aging or in neurodegenerative dementias similar to memory or other cognitive functions. Acetylcholine signaling is crucial for executive function and also diminishes with aging. Acetylcholine’s contribution to the aging- or dementia-related decline in inhibitory control, however, remains elusive. We addressed this in Drosophila using a Go/No-Go task that measures inhibition capacity. Here, we report that inhibition capacity declines with aging in wild-type flies, which is mitigated by lessening acetylcholine breakdown and augmented by reducing acetylcholine biosynthesis. We identified the mushroom body (MB) γ neurons as a chief neural site for acetylcholine’s contribution to the aging-associated inhibitory control deficit. In addition, we found that the MB output neurons MBON-γ2α’1 having dendrites at the MB γ2 and α’1 lobes and axons projecting to the superior medial protocerebrum and the crepine is critical for sustained movement suppression per se. This study reveals, for the first time, the central role of acetylcholine in the aging-associated loss of inhibitory control and provides a framework for further mechanistic studies.

show abstract

Mushroom body output differentiates memory processes and distinct memory-guided behaviors

Cited by 14 publications

References 75 publications

Associative learning drives longitudinally graded presynaptic plasticity of neurotransmitter release along axonal compartments

Associative learning drives longitudinally graded presynaptic plasticity of neurotransmitter release along axonal compartments

Neural circuit mechanisms for transforming learned olfactory valences into wind-oriented movement

Acetylcholine deficit causes dysfunctional inhibitory control in an aging-dependent manner

Contact Info

Product

Resources

About