Effects of short-term plasticity in early olfactory information processing in Drosophila

In Drosophila, olfactory information received by the olfactory receptor neurons (ORNs) is first processed by an incoherent feed forward neural circuit in the antennal lobe (AL) that consists of ORNs (input), the inhibitory local neurons (LNs), and projection neurons (PNs). This "early" olfactory information process has two important characteristics. First, response of a PN to its cognate ORN is normalized by the overall activity of other ORNs, a phenomenon termed "divisive normalization". Second, PNs respond strongly to the onset of ORN activities, but they adapt to prolonged or continuously increasing inputs. Despite the importance of these characteristics for learning and memory, their underlying mechanism remains not fully understood. Here, we develop a circuit model for describing the ORN-LN-PN dynamics by including key features of neuron-neuron interactions, in particular short-term plasticity (STP) and presynaptic inhibition (PI).Our model shows that STP is critical in shaping PN's steady-state response properties. By fitting our model to experimental data quantitatively, we found that strong and balanced short-term facilitation (STF) and short-term depression (STD) in STP is crucial for the observed nonlinear divisive normalization in Drosophila. By comparing our model with the observed adaptive response to time-varying signals quantitatively, we find that both STP and PI contribute to the highly adaptive response with the latter being the dominant factor for a better fit with experimental data. Our model not only helps reveal the mechanisms underlying two main characteristics of the early olfactory process, it can also be used to predict the PN responses to arbitrary time-dependent signals and to infer microscopic properties of the circuit (such as the strengths of STF and STD) from the measured input-output relation.

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Short-Term Plasticity Regulates Both Divisive Normalization and Adaptive Responses in Drosophila Olfactory System

Frontiers in Computational Neuroscience ◽

10.3389/fncom.2021.730431 ◽

2021 ◽

Vol 15 ◽

Author(s):

Yuxuan Liu ◽

Qianyi Li ◽

Chao Tang ◽

Shanshan Qin ◽

Yuhai Tu

Keyword(s):

Experimental Data ◽

Adaptive Response ◽

Neural Circuit ◽

Circuit Model ◽

Projection Neurons ◽

Adaptive Responses ◽

Short Term ◽

Short Term Plasticity ◽

Olfactory Information ◽

Divisive Normalization

In Drosophila, olfactory information received by olfactory receptor neurons (ORNs) is first processed by an incoherent feed forward neural circuit in the antennal lobe (AL) that consists of ORNs (input), inhibitory local neurons (LNs), and projection neurons (PNs). This “early” olfactory information processing has two important characteristics. First, response of a PN to its cognate ORN is normalized by the overall activity of other ORNs, a phenomenon termed “divisive normalization.” Second, PNs respond strongly to the onset of ORN activities, but they adapt to prolonged or continuously varying inputs. Despite the importance of these characteristics for learning and memory, their underlying mechanisms are not fully understood. Here, we develop a circuit model for describing the ORN-LN-PN dynamics by including key neuron-neuron interactions such as short-term plasticity (STP) and presynaptic inhibition (PI). By fitting our model to experimental data quantitatively, we show that a strong STP balanced between short-term facilitation (STF) and short-term depression (STD) is responsible for the observed nonlinear divisive normalization in Drosophila. Our circuit model suggests that either STP or PI alone can lead to adaptive response. However, by comparing our model results with experimental data, we find that both STP and PI work together to achieve a strong and robust adaptive response. Our model not only helps reveal the mechanisms underlying two main characteristics of the early olfactory process, it can also be used to predict PN responses to arbitrary time-dependent signals and to infer microscopic properties of the circuit (such as the strengths of STF and STD) from the measured input-output relation. Our circuit model may be useful for understanding the role of STP in other sensory systems.

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Muscarinic presynaptic modulation in GABAergic pallidal synapses of the rat

Journal of Neurophysiology ◽

10.1152/jn.00385.2014 ◽

2015 ◽

Vol 113 (3) ◽

pp. 796-807 ◽

Cited By ~ 7

Author(s):

Ricardo Hernández-Martínez ◽

José J. Aceves ◽

Pavel E. Rueda-Orozco ◽

Teresa Hernández-Flores ◽

Omar Hernández-González ◽

...

Keyword(s):

Receptor Agonist ◽

Projection Neurons ◽

Quantal Content ◽

Short Term ◽

Paired Pulse ◽

Short Term Plasticity ◽

Striatal Projection Neurons ◽

Muscarinic Cholinergic ◽

Muscarinic Modulation

The external globus pallidus (GPe) is central for basal ganglia processing. It expresses muscarinic cholinergic receptors and receives cholinergic afferents from the pedunculopontine nuclei (PPN) and other regions. The role of these receptors and afferents is unknown. Muscarinic M1-type receptors are expressed by synapses from striatal projection neurons (SPNs). Because axons from SPNs project to the GPe, one hypothesis is that striatopallidal GABAergic terminals may be modulated by M1 receptors. Alternatively, some M1 receptors may be postsynaptic in some pallidal neurons. Evidence of muscarinic modulation in any of these elements would suggest that cholinergic afferents from the PPN, or other sources, could modulate the function of the GPe. In this study, we show this evidence using striatopallidal slice preparations: after field stimulation in the striatum, the cholinergic muscarinic receptor agonist muscarine significantly reduced the amplitude of inhibitory postsynaptic currents (IPSCs) from synapses that exhibited short-term synaptic facilitation. This inhibition was associated with significant increases in paired-pulse facilitation, and quantal content was proportional to IPSC amplitude. These actions were blocked by atropine, pirenzepine, and mamba toxin-7, suggesting that receptors involved were M1. In addition, we found that some pallidal neurons have functional postsynaptic M1 receptors. Moreover, some evoked IPSCs exhibited short-term depression and a different kind of modulation: they were indirectly modulated by muscarine via the activation of presynaptic cannabinoid CB1 receptors. Thus pallidal synapses presenting distinct forms of short-term plasticity were modulated differently.

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Dual Nitrergic/Cholinergic Control of Short-Term Plasticity of Corticostriatal Inputs to Striatal Projection Neurons

Frontiers in Cellular Neuroscience ◽

10.3389/fncel.2015.00453 ◽

2015 ◽

Vol 9 ◽

Cited By ~ 6

Author(s):

Craig P. Blomeley ◽

Sarah Cains ◽

Enrico Bracci

Keyword(s):

Projection Neurons ◽

Short Term ◽

Short Term Plasticity ◽

Striatal Projection Neurons ◽

Corticostriatal Inputs

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Neuropilin 2 signaling mediates corticostriatal transmission, spine maintenance, and goal-directed learning in mice

10.1101/659342 ◽

2019 ◽

Author(s):

Maxime Assous ◽

Edward Martinez ◽

Carol Eisenberg ◽

Aleksandra Kosc ◽

Kristie Varghese ◽

...

Keyword(s):

Dendritic Spines ◽

Neurodevelopmental Disorders ◽

Sensorimotor Learning ◽

Projection Neurons ◽

Short Term ◽

Short Term Plasticity ◽

Guidance Cue ◽

Semaphorin 3F ◽

Directed Learning ◽

Layer V

AbstractThe striatum represents the main input structure of the basal ganglia, receiving massive excitatory input from the cortex and the thalamus. The development and maintenance of cortical input to the striatum is crucial for all striatal function including many forms of sensorimotor integration, learning and action control. The molecular mechanisms regulating the development and maintenance of corticostriatal synaptic transmission are unclear. Here we show that the guidance cue, Semaphorin 3F and its receptor Neuropilin 2 (Nrp2), influence dendritic spine maintenance, corticostriatal short-term plasticity, and learning in adult male and female mice. We found that Nrp2 is enriched in adult layer V pyramidal neurons, corticostriatal terminals, and in developing and adult striatal spiny projection neurons (SPNs). Loss of Nrp2 increases SPN excitability and spine number, reduces short-term facilitation at corticostriatal synapses, and impairs goal-directed learning in an instrumental task. Acute deletion of Nrp2 selectively in adult layer V cortical neurons produces a similar increase in the number of dendritic spines and presynaptic modifications at the corticostriatal synapse in the Nrp2-/- mouse, but does not affect the intrinsic excitability of SPNs. Furthermore conditional loss of Nrp2 impairs sensorimotor learning on the accelerating rotarod without affecting goal-directed instrumental learning. Collectively, our results identify Nrp2 signaling as essential for the development and maintenance of the corticostriatal pathway and may shed novel insights on neurodevelopmental disorders linked to the corticostriatal pathway and semaphorin signaling.Significance StatementThe corticostriatal pathway controls sensorimotor, learning and action control behaviors and its dysregulation is linked to neurodevelopmental disorders, such as autism spectrum disorder (ASD). Here we demonstrate that neuropilin 2 (Nrp2), a receptor for the axon-guidance cue semaphorin 3F, has important and previously unappreciated functions in the development and adult maintenance of dendritic spines on striatal spiny projection neurons (SPNs), corticostriatal short-term plasticity, intrinsic physiological properties of SPNs and learning in mice. Our findings, coupled with Nrp2’s association with ASD in human populations, suggest that Nrp2 may play an important role in ASD pathophysiology. Overall, our work demonstrates Nrp2 as a key regulator of corticostriatal development, maintenance and function, and may lead to better understanding of neurodevelopmental disease mechanisms.

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Short-term plasticity shapes activity pattern-dependent striato-pallidal synaptic transmission

Journal of Neurophysiology ◽

10.1152/jn.00459.2012 ◽

2013 ◽

Vol 109 (4) ◽

pp. 932-939 ◽

Cited By ~ 10

Author(s):

Juhyon Kim ◽

Hitoshi Kita

Keyword(s):

Synaptic Transmission ◽

Firing Pattern ◽

Brain Slice ◽

Projection Neurons ◽

Short Term ◽

Short Term Plasticity ◽

Pathological Conditions ◽

Rat Brain Slice ◽

Signal Transfer Function

The cortico-striato (Str)-globus pallidus external segment (GPe) projection plays major roles in the control of neuronal activity in the basal ganglia under both normal and pathological conditions. The present study used rat brain-slice preparations to address our hypothesis that the gain of this disynaptic projection is dynamically controlled by activations of short-term plasticity mechanisms of Str-GPe synapses. The Str-GPe projection neurons fire with very different frequency and firing patterns in vivo depending on the condition of the animal. The results show that the Str-GPe synapses have very strong short-term enhancement mechanisms and that repetitive burst activation of the Str-GPe synapses, which mimic oscillatory burst firing of Str neurons, can sustain enhanced states of synaptic transmission for tens of seconds. The results reveal that the short-term enhancement of Str-GPe synapses contributes to the generation of pauses in the firing of GPe neurons and that signal transfer function in the Str-GPe projection is highly dependent on the firing pattern of Str neurons.

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