scholarly journals Structural and Functional Plasticity in the Regenerating Olfactory System of the Migratory Locust

2020 ◽  
Vol 11 ◽  
Author(s):  
Gerd Bicker ◽  
Michael Stern

Regeneration after injury is accompanied by transient and lasting changes in the neuroarchitecture of the nervous system and, thus, a form of structural plasticity. In this review, we introduce the olfactory pathway of a particular insect as a convenient model to visualize neural regeneration at an anatomical level and study functional recovery at an electrophysiological level. The olfactory pathway of the locust (Locusta migratoria) is characterized by a multiglomerular innervation of the antennal lobe by olfactory receptor neurons. These olfactory afferents were axotomized by crushing the base of the antenna. The resulting degeneration and regeneration in the antennal lobe could be quantified by size measurements, dye labeling, and immunofluorescence staining of cell surface proteins implicated in axonal guidance during development. Within 3 days post lesion, the antennal lobe volume was reduced by 30% and from then onward regained size back to normal by 2 weeks post injury. The majority of regenerating olfactory receptor axons reinnervated the glomeruli of the antennal lobe. A few regenerating axons project erroneously into the mushroom body on a pathway that is normally chosen by second-order projection neurons. Based on intracellular responses of antennal lobe output neurons to odor stimulation, regenerated fibers establish functional synapses again. Following complete absence after nerve crush, responses to odor stimuli return to control level within 10–14 days. On average, regeneration of afferents, and re-established synaptic connections appear faster in younger fifth instar nymphs than in adults. The initial degeneration of olfactory receptor axons has a trans-synaptic effect on a second order brain center, leading to a transient size reduction of the mushroom body calyx. Odor-evoked oscillating field potentials, absent after nerve crush, were restored in the calyx, indicative of regenerative processes in the network architecture. We conclude that axonal regeneration in the locust olfactory system appears to be possible, precise, and fast, opening an avenue for future mechanistic studies. As a perspective of biomedical importance, the current evidence for nitric oxide/cGMP signaling as positive regulator of axon regeneration in connectives of the ventral nerve cord is considered in light of particular regeneration studies in vertebrate central nervous systems.

Author(s):  
Philipp Schlegel ◽  
Alexander Shakeel Bates ◽  
Tomke Stürner ◽  
Sridhar R. Jagannathan ◽  
Nikolas Drummond ◽  
...  

AbstractThe hemibrain connectome (Scheffer et al., 2020) provides large scale connectivity and morphology information for the majority of the central brain of Drosophila melanogaster. Using this data set, we provide a complete description of the most complex olfactory system studied at synaptic resolution to date, covering all first, second and third-order neurons of the olfactory system associated with the antennal lobe and lateral horn (mushroom body neurons are described in a parallel paper, (Li et al., 2020)). We develop a generally applicable strategy to extract information flow and layered organisation from synaptic resolution connectome graphs, mapping olfactory input to descending interneurons. This identifies a range of motifs including highly lateralised circuits in the antennal lobe and patterns of convergence downstream of the mushroom body and lateral horn. We also leverage a second data set (FAFB, (Zheng et al., 2018)) to provide a first quantitative assessment of inter- versus intra-individual stereotypy. Complete reconstruction of select developmental lineages in two brains (three brain hemispheres) reveals striking similarity in neuronal morphology across brains for >170 cell types. Within and across brains, connectivity correlates with morphology. Notably, neurons of the same morphological type show similar connection variability within one brain as across brains; this property should enable a rigorous quantitative approach to cell typing.


Author(s):  
Jürgen Rybak ◽  
Bill S. Hansson

In the vinegar fly (Drosophila melanogaster), the neuronal pathway that processes olfactory information is organized into multiple layers: a peripheral set of olfactory sensory neurons (OSNs); the primary olfactory center, or antennal lobe (AL); and two second-order neuropils, the mushroom body (MB) and lateral horn (LH). Odorants are detected by the dendrites of OSNs housed in sensilla on the maxillary palps and antennae. The OSN axons converge onto spherical synaptic neuropil within the AL termed glomeruli. OSNs that express the same odorant receptor project to the same glomerulus in a one-to-one fashion, forming discrete olfactory pathways. In the AL, a network of local interneurons (LNs) and projection neurons (PNs) contribute to the first-order processing within the glomeruli. Two types of PNs constitute the principal, parallel output pathways made by PN axons that end in the second-order neuropils of the MB and LH: uniglomerular PNs (uPNs) and multiglomerular PNs (mPNs).


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Gregor A. Bergmann ◽  
Gerd Bicker

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.


2018 ◽  
Author(s):  
Sandhya Mogily ◽  
Meenakshi VijayKumar ◽  
Sunil Kumar Sethy ◽  
Joby Joseph

AbstractThe European honeybee, Apis mellifera is the most common insect model system for studying learning and memory. We establish that the olfactory system of Apis dorsata, an Asian species of honeybee as an equivalent model to Apis mellifera to study physiology underlying learning and memory. We created an Atlas of the antennal lobe and counted the number of glomeruli in the antennal lobe of Apis dorsata to be around 165 which is similar to the number in the other honey bee species Apis mellifera and Apis florea. Apis dorsata was found to have five antenno-cerebral tracts namely mACT, lACT and 3 mlACTS which appear identical to Apis mellifera. Intracellular recording showed that the antennal lobe interneurons exhibit temporally patterned odor-cell specific responses. The neuritis of Kenyon cells with cell bodies located in a neighborhood in calyx retain their relative neighborhoods in the peduncle and alpha lobe forming a columnar organization in the mushroom body. Alpha lobe and the calyx of the mushroom body were innervated by extrinsic neurons with cell bodies in the lateral protocerebrum. A set of GABA positive cells in the lateral protocerebrum send their neurites towards alpha-lobe. Apis dorsata was amenable to olfactory conditioning and showed good learning and memory retention at 24 hours. They were amenable to massed and spaced conditioning and could distinguish trained odor from an untrained novel odor.


2020 ◽  
Author(s):  
Mario Pannunzi ◽  
Thomas Nowotny

AbstractWhen flies explore their environment, they encounter odors in complex, highly intermittent plumes. To navigate a plume and, for example, find food, flies must solve several tasks, including reliably identifying mixtures of odorants and discriminating odorant mixtures emanating from a single source from odorants emitted from separate sources and mixing in the air. Lateral inhibition in the antennal lobe is commonly understood to help solving these two tasks. With a computational model of the Drosophila olfactory system, we analyze the utility of an alternative mechanism for solving them: Non-synaptic (“ephaptic”) interactions (NSIs) between olfactory receptor neurons that are stereotypically co-housed in the same sensilla. For both tasks, NSIs improve the insect olfactory system and outperform the standard lateral inhibition mechanism in the antennal lobe. These results shed light, from an evolutionary perspective, on the role of NSIs, which are normally avoided between neurons, for instance by myelination.


2021 ◽  
Author(s):  
Gregor A. Bergmann ◽  
Gerd Bicker

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.


2010 ◽  
Vol 103 (4) ◽  
pp. 2185-2194 ◽  
Author(s):  
Nina Deisig ◽  
Martin Giurfa ◽  
Jean Christophe Sandoz

Local networks within the primary olfactory centers reformat odor representations from olfactory receptor neurons to second-order neurons. By studying the rules underlying mixture representation at the input to the antennal lobe (AL), the primary olfactory center of the insect brain, we recently found that mixture representation follows a strict elemental rule in honeybees: the more a component activates the AL when presented alone, the more it is represented in a mixture. We now studied mixture representation at the output of the AL by imaging a population of second-order neurons, which convey AL processed odor information to higher brain centers. We systematically measured odor-evoked activity in 22 identified glomeruli in response to four single odorants and all their possible binary, ternary and quaternary mixtures. By comparing input and output responses, we determined how the AL network reformats mixture representation and what advantage this confers for odor discrimination. We show that increased inhibition within the AL leads to more synthetic, less elemental, mixture representation at the output level than that at the input level. As a result, mixture representations become more separable in the olfactory space, thus allowing better differentiation among floral blends in nature.


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