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Olfactory learning skews mushroom body output pathways to steer behavioral choice in Drosophila.

Owald D, Waddell S - Curr. Opin. Neurobiol. (2015)

Bottom Line: How this information is coded in neural networks in the brain, and appropriately retrieved and utilized to guide behavior, is poorly understood.In the fruit fly olfactory memories of particular value are represented within sparse populations of odor-activated Kenyon cells (KCs) in the mushroom body ensemble.Reactivation of this skewed KC-output neuron network retrieves memory of odor valence and guides appropriate approach or avoidance behavior.

View Article: PubMed Central - PubMed

Affiliation: Centre for Neural Circuits and Behaviour, The University of Oxford, Tinsley Building, Mansfield Road, Oxford OX1 3SR, UK.

No MeSH data available.


Related in: MedlinePlus

Model how local feed-forward inhibitory interneurons in the MB could mediate the motivational control of sugar memory retrieval. (a) The MB-MP1 [PPL1-γ1pedc] DANs that innervate the heel and peduncle of the MB provide the inhibitory constraint of satiety on the expression of sugar reward memory [53]. The MB-MP1 presynaptic terminals overlap with the dendrites of the GABAergic MVP2 [MBON-γ1pedc > α/β] (dark blue) [46••] suggesting that MB-MP1 DANs drive plasticity between KC synapses in these regions and the MVP2 MBONs. In the satiated fly the MB-MP1 DANs are tonically active/on and therefore inhibit odor-drive to MVP2, reducing feed-forward inhibition to MBON junctions, such as M4 [MBON-β2 β′2a, MBON-β′2mp] and M6 [MBON-γ5β′2a] outputs on the horizontal lobe tips that drive avoidance. This situation inhibits the expression of reward memories. (b) In hungry flies the MB-MP1 neurons are inhibited/turned off by the action of Neuropeptide F [53]. This results in increased odor-drive to MVP2 and therefore more feed-forward inhibition (MVP2 neuron now light blue) to MBON avoidance pathways (dashed red arrows). This situation favors expression of conditioned odor approach behavior. Interestingly, only nutrient-dependent sugar memory expression requires the flies to be hungry [32••] and MVP2 innervates the relevant α1 zone of the MB. Furthermore, water-reinforced memory expression is promoted by thirst and not hunger and the MVP2 neuron does not seem to have an arbor in the γ4 water-reinforcement zone. A similar mechanism could provide state-dependence to visual and tastant memories.
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fig0015: Model how local feed-forward inhibitory interneurons in the MB could mediate the motivational control of sugar memory retrieval. (a) The MB-MP1 [PPL1-γ1pedc] DANs that innervate the heel and peduncle of the MB provide the inhibitory constraint of satiety on the expression of sugar reward memory [53]. The MB-MP1 presynaptic terminals overlap with the dendrites of the GABAergic MVP2 [MBON-γ1pedc > α/β] (dark blue) [46••] suggesting that MB-MP1 DANs drive plasticity between KC synapses in these regions and the MVP2 MBONs. In the satiated fly the MB-MP1 DANs are tonically active/on and therefore inhibit odor-drive to MVP2, reducing feed-forward inhibition to MBON junctions, such as M4 [MBON-β2 β′2a, MBON-β′2mp] and M6 [MBON-γ5β′2a] outputs on the horizontal lobe tips that drive avoidance. This situation inhibits the expression of reward memories. (b) In hungry flies the MB-MP1 neurons are inhibited/turned off by the action of Neuropeptide F [53]. This results in increased odor-drive to MVP2 and therefore more feed-forward inhibition (MVP2 neuron now light blue) to MBON avoidance pathways (dashed red arrows). This situation favors expression of conditioned odor approach behavior. Interestingly, only nutrient-dependent sugar memory expression requires the flies to be hungry [32••] and MVP2 innervates the relevant α1 zone of the MB. Furthermore, water-reinforced memory expression is promoted by thirst and not hunger and the MVP2 neuron does not seem to have an arbor in the γ4 water-reinforcement zone. A similar mechanism could provide state-dependence to visual and tastant memories.

Mentions: Sugar memory is most robustly expressed in hungry flies [53] whereas thirst promotes the expression of water memory [6••]. It seems possible that forming these memories in different zones on the MB provides a simple organizational scaffold onto which additional control can be differentially exerted. The MB-MP1 [PPL1-γ1pedc] DANs provide the inhibitory constraint of satiety on the expression of sugar memory [53]. The MB-MP1 [PPL1-γ1pedc] neurons can also convey short term aversive memory reinforcement [28] suggesting that negative reinforcement and motivational processes are tightly interlinked in the MB. MP1 [PPL1-γ1pedc] neurons have also been implicated in the transition between different memory phases [54, 55] and forgetting [56]. It is interesting to note that the MB-MP1 [PPL1-γ1pedc] neurons occupy the same zones in the heel and peduncle as the GABA-ergic MVP2 [MBON-γ1pedc > α/β], whose activation drives approach behavior [46••]. The anatomy of MVP2 [MBON-γ1pedc > α/β] suggests that they are feed-forward local MB inhibitory interneurons (Figure 3). It therefore seems plausible that the internal state of hunger also skews the balance of MBON pathways so that those favoring approach are preferentially activated by relevant trained odors. In addition, such a function would indicate that the first layer of MBON integration is within the MB itself. It will be important to determine the role of other neurons that connect MBON zones [32••, 36, 37••] and whether the thirst-dependence of water memory expression [6••] involves a similar DAN control mechanism to that of sugar memory. DANs that innervate the tip of the β′ lobe control the thirst dependence of water vapor seeking in naïve flies [6••]. In addition, DANs and MBONs have been implicated in hunger-dependent modulation of naïve responses to carbon dioxide [15•], temperature preference [57, 58], and the regulation of sleep [46]. Therefore, DAN-driven modulation of the MB does not exclusively gate learned behaviors and might more broadly control the expression of state-dependent goal-directed behaviors.


Olfactory learning skews mushroom body output pathways to steer behavioral choice in Drosophila.

Owald D, Waddell S - Curr. Opin. Neurobiol. (2015)

Model how local feed-forward inhibitory interneurons in the MB could mediate the motivational control of sugar memory retrieval. (a) The MB-MP1 [PPL1-γ1pedc] DANs that innervate the heel and peduncle of the MB provide the inhibitory constraint of satiety on the expression of sugar reward memory [53]. The MB-MP1 presynaptic terminals overlap with the dendrites of the GABAergic MVP2 [MBON-γ1pedc > α/β] (dark blue) [46••] suggesting that MB-MP1 DANs drive plasticity between KC synapses in these regions and the MVP2 MBONs. In the satiated fly the MB-MP1 DANs are tonically active/on and therefore inhibit odor-drive to MVP2, reducing feed-forward inhibition to MBON junctions, such as M4 [MBON-β2 β′2a, MBON-β′2mp] and M6 [MBON-γ5β′2a] outputs on the horizontal lobe tips that drive avoidance. This situation inhibits the expression of reward memories. (b) In hungry flies the MB-MP1 neurons are inhibited/turned off by the action of Neuropeptide F [53]. This results in increased odor-drive to MVP2 and therefore more feed-forward inhibition (MVP2 neuron now light blue) to MBON avoidance pathways (dashed red arrows). This situation favors expression of conditioned odor approach behavior. Interestingly, only nutrient-dependent sugar memory expression requires the flies to be hungry [32••] and MVP2 innervates the relevant α1 zone of the MB. Furthermore, water-reinforced memory expression is promoted by thirst and not hunger and the MVP2 neuron does not seem to have an arbor in the γ4 water-reinforcement zone. A similar mechanism could provide state-dependence to visual and tastant memories.
© Copyright Policy - CC BY-NC-ND
Related In: Results  -  Collection

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fig0015: Model how local feed-forward inhibitory interneurons in the MB could mediate the motivational control of sugar memory retrieval. (a) The MB-MP1 [PPL1-γ1pedc] DANs that innervate the heel and peduncle of the MB provide the inhibitory constraint of satiety on the expression of sugar reward memory [53]. The MB-MP1 presynaptic terminals overlap with the dendrites of the GABAergic MVP2 [MBON-γ1pedc > α/β] (dark blue) [46••] suggesting that MB-MP1 DANs drive plasticity between KC synapses in these regions and the MVP2 MBONs. In the satiated fly the MB-MP1 DANs are tonically active/on and therefore inhibit odor-drive to MVP2, reducing feed-forward inhibition to MBON junctions, such as M4 [MBON-β2 β′2a, MBON-β′2mp] and M6 [MBON-γ5β′2a] outputs on the horizontal lobe tips that drive avoidance. This situation inhibits the expression of reward memories. (b) In hungry flies the MB-MP1 neurons are inhibited/turned off by the action of Neuropeptide F [53]. This results in increased odor-drive to MVP2 and therefore more feed-forward inhibition (MVP2 neuron now light blue) to MBON avoidance pathways (dashed red arrows). This situation favors expression of conditioned odor approach behavior. Interestingly, only nutrient-dependent sugar memory expression requires the flies to be hungry [32••] and MVP2 innervates the relevant α1 zone of the MB. Furthermore, water-reinforced memory expression is promoted by thirst and not hunger and the MVP2 neuron does not seem to have an arbor in the γ4 water-reinforcement zone. A similar mechanism could provide state-dependence to visual and tastant memories.
Mentions: Sugar memory is most robustly expressed in hungry flies [53] whereas thirst promotes the expression of water memory [6••]. It seems possible that forming these memories in different zones on the MB provides a simple organizational scaffold onto which additional control can be differentially exerted. The MB-MP1 [PPL1-γ1pedc] DANs provide the inhibitory constraint of satiety on the expression of sugar memory [53]. The MB-MP1 [PPL1-γ1pedc] neurons can also convey short term aversive memory reinforcement [28] suggesting that negative reinforcement and motivational processes are tightly interlinked in the MB. MP1 [PPL1-γ1pedc] neurons have also been implicated in the transition between different memory phases [54, 55] and forgetting [56]. It is interesting to note that the MB-MP1 [PPL1-γ1pedc] neurons occupy the same zones in the heel and peduncle as the GABA-ergic MVP2 [MBON-γ1pedc > α/β], whose activation drives approach behavior [46••]. The anatomy of MVP2 [MBON-γ1pedc > α/β] suggests that they are feed-forward local MB inhibitory interneurons (Figure 3). It therefore seems plausible that the internal state of hunger also skews the balance of MBON pathways so that those favoring approach are preferentially activated by relevant trained odors. In addition, such a function would indicate that the first layer of MBON integration is within the MB itself. It will be important to determine the role of other neurons that connect MBON zones [32••, 36, 37••] and whether the thirst-dependence of water memory expression [6••] involves a similar DAN control mechanism to that of sugar memory. DANs that innervate the tip of the β′ lobe control the thirst dependence of water vapor seeking in naïve flies [6••]. In addition, DANs and MBONs have been implicated in hunger-dependent modulation of naïve responses to carbon dioxide [15•], temperature preference [57, 58], and the regulation of sleep [46]. Therefore, DAN-driven modulation of the MB does not exclusively gate learned behaviors and might more broadly control the expression of state-dependent goal-directed behaviors.

Bottom Line: How this information is coded in neural networks in the brain, and appropriately retrieved and utilized to guide behavior, is poorly understood.In the fruit fly olfactory memories of particular value are represented within sparse populations of odor-activated Kenyon cells (KCs) in the mushroom body ensemble.Reactivation of this skewed KC-output neuron network retrieves memory of odor valence and guides appropriate approach or avoidance behavior.

View Article: PubMed Central - PubMed

Affiliation: Centre for Neural Circuits and Behaviour, The University of Oxford, Tinsley Building, Mansfield Road, Oxford OX1 3SR, UK.

No MeSH data available.


Related in: MedlinePlus