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

ABSTRACT: The relatively large primary olfactory center of the insect brain, the antennal lobe (AL), contains several heterogeneous neuronal types. These include projection neurons (PNs), providing olfactory information to higher-order neuropils via parallel pathways, and local interneurons (LNs), which provide lateral processing within the AL. In addition, various types of centrifugal neurons (CNs) offer top-down modulation onto the other AL neurons. By performing iontophoretic intracellular staining, we collected a large number of AL neurons in the moth, Helicoverpa armigera, to examine the distinct morphological features of PNs, LNs, and CNs. We characterize 190 AL neurons. These were allocated to 25 distinct neuronal types or sub-types, which were reconstructed and placed into a reference brain. In addition to six PN types comprising 15 sub-types, three LN and seven CN types were identified. High-resolution confocal images allowed us to analyze AL innervations of the various reported neurons, which demonstrated that all PNs innervating ventroposterior glomeruli contact a protocerebral neuropil rarely targeted by other PNs, that is the posteriorlateral protocerebrum. We also discuss the functional roles of the distinct CNs, which included several previously uncharacterized types, likely involved in computations spanning from multisensory processing to olfactory feedback signalization into the AL.

SUBMITTER: Kymre JH

PROVIDER: S-EPMC8048870 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Projection-neurons (PNs) within the antennal lobe (AL) of the hawkmoth respond vigorously to odor stimulation, with each vigorous response followed by a ~1 s period of suppression-dubbed the "afterhyperpolarization-phase," or AHP-phase. Prior evidence indicates that this AHP-phase is important for the processing of odors, but the mechanisms underlying this phase and its function remain unknown. We investigate this issue. Beginning with several physiological experiments, we find that pharmacological manipulation of the AL yields surprising results. Specifically, (a) the application of picrotoxin (PTX) lengthens the AHP-phase and reduces PN activity, whereas (b) the application of Bicuculline-methiodide (BIC) reduces the AHP-phase and increases PN activity. These results are curious, as both PTX and BIC are inhibitory-receptor antagonists. To resolve this conundrum, we speculate that perhaps (a) PTX reduces PN activity through a disinhibitory circuit involving a heterogeneous population of local-neurons, and (b) BIC acts to hamper certain intrinsic currents within the PNs that contribute to the AHP-phase. To probe these hypotheses further we build a computational model of the AL and benchmark our model against our experimental observations. We find that, for parameters which satisfy these benchmarks, our model exhibits a particular kind of synchronous activity: namely, "multiple-firing-events" (MFEs). These MFEs are causally-linked sequences of spikes which emerge stochastically, and turn out to have important dynamical consequences for all the experimentally observed phenomena we used as benchmarks. Taking a step back, we extract a few predictions from our computational model pertaining to the real AL: Some predictions deal with the MFEs we expect to see in the real AL, whereas other predictions involve the runaway synchronization that we expect when BIC-application hampers the AHP-phase. By examining the literature we see support for the former, and we perform some additional experiments to confirm the latter. The confirmation of these predictions validates, at least partially, our initial speculation above. We conclude that the AL is poised in a state of high-gain; ready to respond vigorously to even faint stimuli. After each response the AHP-phase functions to prevent runaway synchronization and to "reset" the AL for another odor-specific response.

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

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