Abstract
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.
Highlights
It has long been understood that recurrent connectivity as well as intrinsic cellular properties both play a role in the dynamics of the insect Antennal Lobe (AL) (Hansson and Anton, 2000; Vosshall et al, 2000; Assisi et al, 2007; Galizia and Rössler, 2010)
If our picture is accurate and the Manduca AL does exhibit the mechanisms we propose, we are lead naturally to the grander question: what purpose could they serve? We hypothesize that perhaps the Manduca has evolved to excel at certain difficult sensory tasks, such as finding a mate on the wing through a highly dynamic scent plume
One necessary computation for such behavior would be to reliably detect and respond to a faint odor-filament spun across a turbulent breeze. It encounters such filaments intermittently, with each brief exposure to pheromone lasting no more than a few 10 s of millisecond, and with subsequent glimpses of the odor separated by several 100 s of millisecond. In this kind of scenario it makes some amount of sense for the AL to be in a very highgain state; with even the slightest hint of pheromone eliciting a vigorous response
Summary
It has long been understood that recurrent connectivity as well as intrinsic cellular properties both play a role in the dynamics of the insect Antennal Lobe (AL) (Hansson and Anton, 2000; Vosshall et al, 2000; Assisi et al, 2007; Galizia and Rössler, 2010). The Manduca AL itself houses many interneurons, including both Local Neurons (LNs) as well as Projection Neurons (PNs) which send information further downstream (Homberg et al, 1989; Lei et al, 2010) These neurons are organized into functional and morphological modules—a.k.a. glomeruli—which are each stimulated by different classes of odorants. In this paper we largely concentrate on two such glomeruli—named the “cumulus” and “toroid” in male moth—which form the so-called Macroglomerular Complex (MGC) (Matsumoto and Hildebrand, 1981; Christensen and Hildebrand, 1987) This MGC serves as the first central stage of detection and processing of conspecific female sex-pheromones, and plays a crucial role in many of the Manduca’s mating behaviors (Schneiderman et al, 1986; Hansson et al, 1991)
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
