Antennal‐lobe neurons in the moth Helicoverpa armigera : Morphological features of projection neurons, local interneurons, and centrifugal neurons

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.

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

Neuron Glia Biology ◽

10.1017/s1740925x12000075 ◽

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.

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Transient voltage-activated K+ currents in central antennal lobe neurons: cell type-specific functional properties

Journal of Neurophysiology ◽

10.1152/jn.00685.2016 ◽

2017 ◽

Vol 117 (5) ◽

pp. 2053-2064 ◽

Cited By ~ 2

Author(s):

Lars Paeger ◽

Viktor Bardos ◽

Peter Kloppenburg

Keyword(s):

Functional Properties ◽

Antennal Lobe ◽

Projection Neurons ◽

Cell Type ◽

Electrophysiological Properties ◽

Olfactory Information ◽

Local Interneurons ◽

Cell Type Specific ◽

Transient Voltage ◽

Marked Cell

In this study we analyzed transient voltage-activated K+ currents ( IA) of projection neurons and local interneurons in the antennal lobe of the cockroach Periplaneta americana. The antennal lobe is the first synaptic processing station for olfactory information in insects. Local interneurons are crucial for computing olfactory information and form local synaptic connections exclusively in the antennal lobe, whereas a primary task of the projection neurons is the transfer of preprocessed olfactory information from the antennal lobe to higher order centers in the protocerebrum. The different physiological tasks of these neurons require specialized physiological and morphological neuronal phenotypes. We asked if and how the different physiological phenotypes are reflected in the functional properties of IA, which is crucial for shaping intrinsic electrophysiological properties of neurons. Whole cell patch-clamp recordings from adult male P. americana showed that all their central antennal lobe neurons can generate IA. The current exhibited marked cell type-specific differences in voltage dependence of steady-state activation and inactivation, and differences in inactivation kinetics during sustained depolarization. Pharmacological experiments revealed that IA in all neuron types was partially blocked by α-dendrotoxin and phrixotoxin-2, which are considered blockers with specificity for Shaker- and Shal-type channels, respectively. These findings suggest that IA in each cell type is a mixed current generated by channels of both families. The functional role of IA was analyzed in experiments under current clamp, in which portions of IA were blocked by α-dendrotoxin or phrixotoxin-2. These experiments showed that IA contributes significantly to the intrinsic electrophysiological properties, such as the action potential waveform and membrane excitability. NEW & NOTEWORTHY In the insect olfactory system, projection neurons and local interneurons have task-specific electrophysiological and morphological phenotypes. Voltage-activated potassium channels play a crucial role in shaping functional properties of these neurons. This study revealed marked cell type-specific differences in the biophysical properties of transient voltage-activated potassium currents in central antennal lobe neurons.

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Odor processing in the cockroach antennal lobe—the network components

Cell and Tissue Research ◽

10.1007/s00441-020-03387-3 ◽

2021 ◽

Vol 383 (1) ◽

pp. 59-73

Author(s):

Debora Fuscà ◽

Peter Kloppenburg

Keyword(s):

Antennal Lobe ◽

Periplaneta Americana ◽

Experimental System ◽

Projection Neurons ◽

Odor Processing ◽

Local Interneurons ◽

Physiological Properties ◽

Functional Equivalent ◽

The Central Nervous System ◽

Physiological Tasks

AbstractHighly interconnected neural networks perform olfactory signal processing in the central nervous system. In insects, the first synaptic processing of the olfactory input from the antennae occurs in the antennal lobe, the functional equivalent of the olfactory bulb in vertebrates. Key components of the olfactory network in the antennal lobe are two main types of neurons: the local interneurons and the projection (output) neurons. Both neuron types have different physiological tasks during olfactory processing, which accordingly require specialized functional phenotypes. This review gives an overview of important cell type-specific functional properties of the different types of projection neurons and local interneurons in the antennal lobe of the cockroach Periplaneta americana, which is an experimental system that has elucidated many important biophysical and cellular bases of intrinsic physiological properties of these neurons.

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