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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

A piano-playing model for learned valence in the KC-MBON network. (a) The canonical view on higher order processing in the fly brain places the LH (not shown) as instrumental for the expression of innate odor-driven behaviors. Experiments blocking all synaptic output from KCs either by ablation or acute silencing suggested the MBs were dispensable for innate odor-driven behavior, but essential for learned responses. However recent findings demonstrate that blocking the MBONs from the tips of the horizontal MB lobes radically alters naïve and learned odor-driven behaviors [13••, 15•]. In addition, the activity of particular MBONs is now known to favor either avoidance (red arrows) or approach (green arrows) [13••, 46••]. It therefore seems logical that the contribution of these MBONs is integrated and balanced in the naïve fly, leading to an apparent lack of contribution from the MB and neutrality in naïve odor-driven tasks. For simplicity we illustrated the balance as equal numbers of outputs (4 plus and 4 minus = zero, neutrality), but it need only be balanced by the relative weights. (b) Reward learning with sugar depresses the odor-specific KC connections to avoidance MBONs (black arrows). In addition it modulates/enhances approach connections (thicker green arrow). This skewed balance (4 plus and 1 minus) now favors odor-driven approach. (c) Aversive conditioning depresses the odor-specific KC connections to approach MBONs (black arrows). In addition it enhances avoidance connections (thicker red arrow). This skewed balance (1 plus and 4 minus) now favors odor-driven avoidance. Avoidance neurons are glutamatergic whereas approach neurons are cholinergic or GABAergic [13••, 46••].
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fig0010: A piano-playing model for learned valence in the KC-MBON network. (a) The canonical view on higher order processing in the fly brain places the LH (not shown) as instrumental for the expression of innate odor-driven behaviors. Experiments blocking all synaptic output from KCs either by ablation or acute silencing suggested the MBs were dispensable for innate odor-driven behavior, but essential for learned responses. However recent findings demonstrate that blocking the MBONs from the tips of the horizontal MB lobes radically alters naïve and learned odor-driven behaviors [13••, 15•]. In addition, the activity of particular MBONs is now known to favor either avoidance (red arrows) or approach (green arrows) [13••, 46••]. It therefore seems logical that the contribution of these MBONs is integrated and balanced in the naïve fly, leading to an apparent lack of contribution from the MB and neutrality in naïve odor-driven tasks. For simplicity we illustrated the balance as equal numbers of outputs (4 plus and 4 minus = zero, neutrality), but it need only be balanced by the relative weights. (b) Reward learning with sugar depresses the odor-specific KC connections to avoidance MBONs (black arrows). In addition it modulates/enhances approach connections (thicker green arrow). This skewed balance (4 plus and 1 minus) now favors odor-driven approach. (c) Aversive conditioning depresses the odor-specific KC connections to approach MBONs (black arrows). In addition it enhances avoidance connections (thicker red arrow). This skewed balance (1 plus and 4 minus) now favors odor-driven avoidance. Avoidance neurons are glutamatergic whereas approach neurons are cholinergic or GABAergic [13••, 46••].

Mentions: The observed learning-related changes of odor-drive to MBONs, and intrinsic valence of particular MBONs support a model wherein learning skews collections of KC-MBON pathways that are ordinarily balanced in naïve flies (Figure 2a). Appetitive learning promotes odor approach by depressing odor-drive to avoidance MBON pathways and perhaps strengthening approach pathways (Figure 2b). In contrast aversive learning promotes odor avoidance by depressing odor-drive to MBON pathways that direct approach while strengthening those for avoidance (Figure 2c). During memory testing, reactivation of these skewed KC-MBON networks by the trained odor retrieves the memory valence and either leads to odor-approach or avoidance behavior.


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

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

A piano-playing model for learned valence in the KC-MBON network. (a) The canonical view on higher order processing in the fly brain places the LH (not shown) as instrumental for the expression of innate odor-driven behaviors. Experiments blocking all synaptic output from KCs either by ablation or acute silencing suggested the MBs were dispensable for innate odor-driven behavior, but essential for learned responses. However recent findings demonstrate that blocking the MBONs from the tips of the horizontal MB lobes radically alters naïve and learned odor-driven behaviors [13••, 15•]. In addition, the activity of particular MBONs is now known to favor either avoidance (red arrows) or approach (green arrows) [13••, 46••]. It therefore seems logical that the contribution of these MBONs is integrated and balanced in the naïve fly, leading to an apparent lack of contribution from the MB and neutrality in naïve odor-driven tasks. For simplicity we illustrated the balance as equal numbers of outputs (4 plus and 4 minus = zero, neutrality), but it need only be balanced by the relative weights. (b) Reward learning with sugar depresses the odor-specific KC connections to avoidance MBONs (black arrows). In addition it modulates/enhances approach connections (thicker green arrow). This skewed balance (4 plus and 1 minus) now favors odor-driven approach. (c) Aversive conditioning depresses the odor-specific KC connections to approach MBONs (black arrows). In addition it enhances avoidance connections (thicker red arrow). This skewed balance (1 plus and 4 minus) now favors odor-driven avoidance. Avoidance neurons are glutamatergic whereas approach neurons are cholinergic or GABAergic [13••, 46••].
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fig0010: A piano-playing model for learned valence in the KC-MBON network. (a) The canonical view on higher order processing in the fly brain places the LH (not shown) as instrumental for the expression of innate odor-driven behaviors. Experiments blocking all synaptic output from KCs either by ablation or acute silencing suggested the MBs were dispensable for innate odor-driven behavior, but essential for learned responses. However recent findings demonstrate that blocking the MBONs from the tips of the horizontal MB lobes radically alters naïve and learned odor-driven behaviors [13••, 15•]. In addition, the activity of particular MBONs is now known to favor either avoidance (red arrows) or approach (green arrows) [13••, 46••]. It therefore seems logical that the contribution of these MBONs is integrated and balanced in the naïve fly, leading to an apparent lack of contribution from the MB and neutrality in naïve odor-driven tasks. For simplicity we illustrated the balance as equal numbers of outputs (4 plus and 4 minus = zero, neutrality), but it need only be balanced by the relative weights. (b) Reward learning with sugar depresses the odor-specific KC connections to avoidance MBONs (black arrows). In addition it modulates/enhances approach connections (thicker green arrow). This skewed balance (4 plus and 1 minus) now favors odor-driven approach. (c) Aversive conditioning depresses the odor-specific KC connections to approach MBONs (black arrows). In addition it enhances avoidance connections (thicker red arrow). This skewed balance (1 plus and 4 minus) now favors odor-driven avoidance. Avoidance neurons are glutamatergic whereas approach neurons are cholinergic or GABAergic [13••, 46••].
Mentions: The observed learning-related changes of odor-drive to MBONs, and intrinsic valence of particular MBONs support a model wherein learning skews collections of KC-MBON pathways that are ordinarily balanced in naïve flies (Figure 2a). Appetitive learning promotes odor approach by depressing odor-drive to avoidance MBON pathways and perhaps strengthening approach pathways (Figure 2b). In contrast aversive learning promotes odor avoidance by depressing odor-drive to MBON pathways that direct approach while strengthening those for avoidance (Figure 2c). During memory testing, reactivation of these skewed KC-MBON networks by the trained odor retrieves the memory valence and either leads to odor-approach or avoidance behavior.

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