scholarly journals Temporally specific engagement of distinct neuronal circuits regulating olfactory habituation in Drosophila

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Ourania Semelidou ◽  
Summer F Acevedo ◽  
Efthimios MC Skoulakis

Habituation is the process that enables salience filtering, precipitating perceptual changes that alter the value of environmental stimuli. To discern the neuronal circuits underlying habituation to brief inconsequential stimuli, we developed a novel olfactory habituation paradigm, identifying two distinct phases of the response that engage distinct neuronal circuits. Responsiveness to the continuous odor stimulus is maintained initially, a phase we term habituation latency and requires Rutabaga Adenylyl-Cyclase-depended neurotransmission from GABAergic Antennal Lobe Interneurons and activation of excitatory Projection Neurons (PNs) and the Mushroom Bodies. In contrast, habituation depends on the inhibitory PNs of the middle Antenno-Cerebral Track, requires inner Antenno-Cerebral Track PN activation and defines a temporally distinct phase. Collectively, our data support the involvement of Lateral Horn excitatory and inhibitory stimulation in habituation. These results provide essential cellular substrates for future analyses of the molecular mechanisms that govern the duration and transition between these distinct temporal habituation phases.Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (<xref ref-type="decision-letter" rid="SA1">see decision letter</xref>).

2016 ◽  
Vol 115 (5) ◽  
pp. 2303-2316 ◽  
Author(s):  
Pavel Sanda ◽  
Tiffany Kee ◽  
Nitin Gupta ◽  
Mark Stopfer ◽  
Maxim Bazhenov

Olfactory processing takes place across multiple layers of neurons from the transduction of odorants in the periphery, to odor quality processing, learning, and decision making in higher olfactory structures. In insects, projection neurons (PNs) in the antennal lobe send odor information to the Kenyon cells (KCs) of the mushroom bodies and lateral horn neurons (LHNs). To examine the odor information content in different structures of the insect brain, antennal lobe, mushroom bodies and lateral horn, we designed a model of the olfactory network based on electrophysiological recordings made in vivo in the locust. We found that populations of all types (PNs, LHNs, and KCs) had lower odor classification error rates than individual cells of any given type. This improvement was quantitatively different from that observed using uniform populations of identical neurons compared with spatially structured population of neurons tuned to different odor features. This result, therefore, reflects an emergent network property. Odor classification improved with increasing stimulus duration: for similar odorants, KC and LHN ensembles reached optimal discrimination within the first 300–500 ms of the odor response. Performance improvement with time was much greater for a population of cells than for individual neurons. We conclude that, for PNs, LHNs, and KCs, ensemble responses are always much more informative than single-cell responses, despite the accumulation of noise along with odor information.


2018 ◽  
Author(s):  
Seong-Gyu Lee ◽  
Christine Fogarty Celestino ◽  
Jeffrey Stagg ◽  
Christoph Kleineidam ◽  
Neil J. Vickers

AbstractOlfactory projection neurons convey information from the insect antennal lobe (AL) to higher centers in the brain. Many studies on moths have reported excitatory projection neurons with cell bodies in the medial cell cluster (mcPNs) that predominantly send an axon from the AL to calyces of the mushroom body (CA) via the medial antennal lobe tract (mALT) and then to the lateral horn (LH) of the protocerebrum. These neurons tend to have dendritic arbors restricted to a single glomerulus (i.e. they are uniglomerular). In this study, we report on the physiological and morphological properties of a group of pheromone-responsive olfactory projection neurons with cell bodies in the moth AL lateral cell cluster (lcPNs) of two heliothine moth species. While mcPNs typically exhibit a narrow odor tuning range related to the restriction of their dendritic arbors within a single glomerulus, lcPNs exhibited an array of morphological and physiological configurations. Pheromone-responsive lcPNs varied in their associations with glomeruli (uniglomerular and multiglomerular), dendritic arborization structure and connections to higher brain centers with projections primarily through the lateral antennal lobe tract and to a lesser extent the mediolateral antennal lobe tract to a variety of protocerebral targets including ventrolateral and superior neuropils as well as LH. Physiological characterization of lcPNs also revealed a diversity of response profiles including those either enhanced by or reliant upon presentation of a pheromone blend. These responses manifested themselves as higher maximum firing rates and/or improved temporal resolution of pulsatile stimuli. lcPNs therefore participate in conveying a variety of olfactory information relating to qualitative and temporal facets of the pheromone stimulus to a more expansive number of protocerebral targets than their mcPN counterparts. The role of lcPNs in the overall scheme of olfactory processing is discussed.


eLife ◽  
2014 ◽  
Vol 3 ◽  
Author(s):  
Timothy J Mosca ◽  
Liqun Luo

Understanding information flow through neuronal circuits requires knowledge of their synaptic organization. In this study, we utilized fluorescent pre- and postsynaptic markers to map synaptic organization in the Drosophila antennal lobe, the first olfactory processing center. Olfactory receptor neurons (ORNs) produce a constant synaptic density across different glomeruli. Each ORN within a class contributes nearly identical active zone number. Active zones from ORNs, projection neurons (PNs), and local interneurons have distinct subglomerular and subcellular distributions. The correct number of ORN active zones and PN acetylcholine receptor clusters requires the Teneurins, conserved transmembrane proteins involved in neuromuscular synapse organization and synaptic partner matching. Ten-a acts in ORNs to organize presynaptic active zones via the spectrin cytoskeleton. Ten-m acts in PNs autonomously to regulate acetylcholine receptor cluster number and transsynaptically to regulate ORN active zone number. These studies advanced our ability to assess synaptic architecture in complex CNS circuits and their underlying molecular mechanisms.


2017 ◽  
Vol 98 ◽  
pp. 214-222 ◽  
Author(s):  
Takuya Nirazawa ◽  
Takeshi Fujii ◽  
Yoichi Seki ◽  
Shigehiro Namiki ◽  
Tomoki Kazawa ◽  
...  

2011 ◽  
Vol 71 ◽  
pp. e79
Author(s):  
Masashi Tabuchi ◽  
Takeshi Sakurai ◽  
Hidefumi Mitsuno ◽  
Shigehiro Namiki ◽  
Ryo Minegishi ◽  
...  

Insects ◽  
2020 ◽  
Vol 11 (1) ◽  
pp. 43 ◽  
Author(s):  
Claudia Groh ◽  
Wolfgang Rössler

Mushroom bodies (MBs) are multisensory integration centers in the insect brain involved in learning and memory formation. In the honeybee, the main sensory input region (calyx) of MBs is comparatively large and receives input from mainly olfactory and visual senses, but also from gustatory/tactile modalities. Behavioral plasticity following differential brood care, changes in sensory exposure or the formation of associative long-term memory (LTM) was shown to be associated with structural plasticity in synaptic microcircuits (microglomeruli) within olfactory and visual compartments of the MB calyx. In the same line, physiological studies have demonstrated that MB-calyx microcircuits change response properties after associative learning. The aim of this review is to provide an update and synthesis of recent research on the plasticity of microcircuits in the MB calyx of the honeybee, specifically looking at the synaptic connectivity between sensory projection neurons (PNs) and MB intrinsic neurons (Kenyon cells). We focus on the honeybee as a favorable experimental insect for studying neuronal mechanisms underlying complex social behavior, but also compare it with other insect species for certain aspects. This review concludes by highlighting open questions and promising routes for future research aimed at understanding the causal relationships between neuronal and behavioral plasticity in this charismatic social insect.


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