scholarly journals Transmitter Co-Expression Reveals Key Organizational Principles of Local Interneuron Heterogeneity in the Olfactory System

2017 ◽  
Author(s):  
Kristyn M. Lizbinski ◽  
Gary F. Marsat ◽  
Andrew M. Dacks
Keyword(s):  
Antennal Lobe ◽  
Expression Patterns ◽  
Receptor Expression ◽  
Projection Neurons ◽  
Local Interneuron ◽  
Local Interneurons ◽  
Receptor Neurons ◽  
Random Probability ◽  
Organizational Principles ◽  
Organizing Principles

AbstractHeterogeneity of individual neurons within a population expands the computational power of the entire neural network. However, the organizing principles that support heterogeneity within a neuronal class are often poorly understood. Here, we focus on a highly heterogeneous population of local interneurons whose traits co-vary seemingly at random. We asked if local interneurons (LNs) in the antennal lobe (AL) of Manduca sexta express fixed, predictable combinations of neurotransmitters, or if transmitter co-expression can be explained by random probability. We systematically determined the co-expression of neuropeptides and GABA by LNs and found variable patterns of co-expression for all neuropeptides, except for tachykininergic LNs which exhibited highly stereotyped co-expression on a neuron-by-neuron basis. To test if observed patterns of co-expression were random, we used a computational model and found that the probabilities of transmitter co-expression cannot be explained by independent expression of each transmitter. We also determined that setting a single rule in the model, while leaving the rest of the co-expression up to random probability, allowed the model to replicate the overall heterogeneity of transmitter co-expression across antennal lobe LNs. This implies that certain co-expression relationships contribute to the ground plan of the AL, but that otherwise, transmitter expression amongst LNs may be random, allowing heterogeneous co-expression patterns to emerge. Furthermore, neuropeptide receptor expression suggests that peptidergic signaling from LNs may simultaneously target olfactory receptor neurons, LNs and projection neurons, and thus the effects of different peptides do not segregate based on principal AL cell type. Our data suggest that while specific constraints may partially shape transmitter co-expression in LNs, a large amount of flexibility on a neuron-by-neuron basis produces heterogeneous network parameters.

scholarly journals A resource for the Drosophila antennal lobe provided by the connectome of glomerulus VA1v

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Jane Anne Horne ◽  
Carlie Langille ◽  
Sari McLin ◽  
Meagan Wiederman ◽  
Zhiyuan Lu ◽  
...  
Keyword(s):  
Drosophila Melanogaster ◽  
Olfactory Receptor ◽  
Antennal Lobe ◽  
Olfactory Receptor Neurons ◽  
Projection Neurons ◽  
Sexually Dimorphic ◽  
Genetic Screens ◽  
Local Interneurons ◽  
Receptor Neurons ◽  
The Right

Using FIB-SEM we report the entire synaptic connectome of glomerulus VA1v of the right antennal lobe in Drosophila melanogaster. Within the glomerulus we densely reconstructed all neurons, including hitherto elusive local interneurons. The fruitless-positive, sexually dimorphic VA1v included >11,140 presynaptic sites with ~38,050 postsynaptic dendrites. These connected input olfactory receptor neurons (ORNs, 51 ipsilateral, 56 contralateral), output projection neurons (18 PNs), and local interneurons (56 of >150 previously reported LNs). ORNs are predominantly presynaptic and PNs predominantly postsynaptic; newly reported LN circuits are largely an equal mixture and confer extensive synaptic reciprocity, except the newly reported LN2V with input from ORNs and outputs mostly to monoglomerular PNs, however. PNs were more numerous than previously reported from genetic screens, suggesting that the latter failed to reach saturation. We report a matrix of 192 bodies each having >50 connections; these form 88% of the glomerulus’ pre/postsynaptic sites.

scholarly journals Local interneurons and projection neurons in the antennal lobe from a spiking point of view

2013 ◽  
Vol 110 (10) ◽  
pp. 2465-2474 ◽  
Author(s):  
Anneke Meyer ◽  
C. Giovanni Galizia ◽  
Martin Paul Nawrot
Keyword(s):  
Antennal Lobe ◽  
Essential Feature ◽  
Point Of View ◽  
Local Network ◽  
Projection Neurons ◽  
Receptor Repertoire ◽  
Local Interneurons ◽  
Spatio Temporal ◽  
Characteristic Features

Local computation in microcircuits is an essential feature of distributed information processing in vertebrate and invertebrate brains. The insect antennal lobe represents a spatially confined local network that processes high-dimensional and redundant peripheral input to compute an efficient odor code. Social insects can rely on a particularly rich olfactory receptor repertoire, and they exhibit complex odor-guided behaviors. This corresponds with a high anatomical complexity of their antennal lobe network. In the honeybee, a large number of glomeruli that receive sensory input are interconnected by a dense network of local interneurons (LNs). Uniglomerular projection neurons (PNs) integrate sensory and recurrent local network input into an efficient spatio-temporal odor code. To investigate the specific computational roles of LNs and PNs, we measured several features of sub- and suprathreshold single-cell responses to in vivo odor stimulation. Using a semisupervised cluster analysis, we identified a combination of five characteristic features as sufficient to separate LNs and PNs from each other, independent of the applied odor-stimuli. The two clusters differed significantly in all these five features. PNs showed a higher spontaneous subthreshold activation, assumed higher peak response rates and a more regular spiking pattern. LNs reacted considerably faster to the onset of a stimulus, and their responses were more reliable across stimulus repetitions. We discuss possible mechanisms that can explain our results, and we interpret cell-type-specific characteristics with respect to their functional relevance.

Direct and glia-mediated effects of GABA on development of central olfactory neurons

2011 ◽  
Vol 7 (2-4) ◽  
pp. 143-161
Author(s):  
Heather S. Mallory ◽  
Nicholas J. Gibson ◽  
Jon H. Hayashi ◽  
Alan J. Nighorn ◽  
Lynne A. Oland
Keyword(s):  
Glial Cells ◽  
Antennal Lobe ◽  
Neuronal Morphology ◽  
Projection Neurons ◽  
Olfactory Pathway ◽  
Mediated Effects ◽  
Local Interneurons ◽  
Outward Currents ◽  
Olfactory Glomeruli

Previously studied for its role in processing olfactory information in the antennal lobe, GABA also may shape development of the olfactory pathway, acting either through or on glial cells. Early in development, the dendrites of GABAergic neurons extend to the glial border that surrounds the nascent olfactory lobe neuropil. These neuropil glia express both GABAA and GABAB receptors, about half of the glia in acute cultures responded to GABA with small outward currents, and about a third responded with small transient increases in intracellular calcium. The neuronal classes that express GABA in vivo, the local interneurons and a subset of projection neurons, also do so in culture. Exposure to GABA in culture increased the size and complexity of local interneurons, but had no effect on glial morphology. The presence of glia alone did not affect neuronal morphology, but in the presence of both glia and GABA, the growth-enhancing effects of GABA on cultured antennal lobe neurons were eliminated. Contact between the glial cells and the neurons was not necessary. Operating in vivo, these antagonistic effects, one direct and one glia mediated, could help to sculpt the densely branched, tufted arbors that are characteristic of neurons innervating olfactory glomeruli.

scholarly journals Cholinergic calcium responses in cultured antennal lobe neurons of the migratory locust

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Gregor A. Bergmann ◽  
Gerd Bicker
Keyword(s):  
Olfactory Receptor ◽  
Intracellular Signaling ◽  
Antennal Lobe ◽  
Locusta Migratoria ◽  
Cytosolic Calcium ◽  
Olfactory Receptor Neurons ◽  
Future Research ◽  
Migratory Locust ◽  
Local Interneurons ◽  
Receptor Neurons

AbstractLocusts are advantageous organisms to elucidate mechanisms of olfactory coding at the systems level. Sensory input is provided by the olfactory receptor neurons of the antenna, which send their axons into the antennal lobe. So far, cellular properties of neurons isolated from the circuitry of the olfactory system, such as transmitter-induced calcium responses, have not been studied. Biochemical and immunocytochemical investigations have provided evidence for acetylcholine as classical transmitter of olfactory receptor neurons. Here, we characterize cell cultured projection and local interneurons of the antennal lobe by cytosolic calcium imaging to cholinergic stimulation. We bulk loaded the indicator dye Cal-520 AM in dissociated culture and recorded calcium transients after applying cholinergic agonists and antagonists. The majority of projection and local neurons respond with increases in calcium levels to activation of both nicotinic and muscarinic receptors. In local interneurons, we reveal interactions lasting over minutes between intracellular signaling pathways, mediated by muscarinic and nicotinic receptor stimulation. The present investigation is pioneer in showing that Cal-520 AM readily loads Locusta migratoria neurons, making it a valuable tool for future research in locust neurophysiology, neuropharmacology, and neurodevelopment.

scholarly journals The wiring logic of an identified serotonergic neuron that spans sensory networks

2020 ◽  
Author(s):  
Kaylynn E. Coates ◽  
Steven A. Calle-Schuler ◽  
Levi M. Helmick ◽  
Victoria L. Knotts ◽  
Brennah N. Martik ◽  
...  
Keyword(s):  
Single Cell ◽  
Synaptic Input ◽  
Antennal Lobe ◽  
Projection Neurons ◽  
Dependent Manner ◽  
Serotonergic Neuron ◽  
Local Interneuron ◽  
Local Networks ◽  
First Order ◽  
Specific Input

AbstractSerotonergic neurons modulate diverse physiological and behavioral processes in a context-dependent manner, based on their complex connectivity. However, their connectivity has not been comprehensively explored at a single-cell resolution. Using a whole-brain EM dataset we determined the wiring logic of a broadly projecting serotonergic neuron (the “CSDn”) in Drosophila. Within the antennal lobe (AL; first-order olfactory region), the CSDn receives glomerulus-specific input and preferentially targets distinct local interneuron subtypes. Furthermore, the wiring logic of the CSDn differs between olfactory regions. The CSDn innervates the AL and lateral horn (LH), yet does not maintain the same synaptic relationship with individual projection neurons that also span both regions. Consistent with this, the CSDn has more distributed connectivity in the LH relative to the AL, preferentially synapsing with principal neuron types based on presumptive transmitter content. Lastly, we identify protocerebral neurons that provide abundant synaptic input to the CSDn. Our study demonstrates how an individual modulatory neuron can interact with local networks and integrate input from non-olfactory sources.

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