Intrinsic and Network Mechanisms Constrain Neural Synchrony in the Moth Antennal Lobe

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.

Effects of Mechanosensory Input on the Tracking of Pulsatile Odor Stimuli by Moth Antennal Lobe Neurons

“…Upon any neuron reaching a threshold voltage of V thres = 1, a spike is recorded and its voltage subsequently reset to V L = 0 (and held at V L = 0 for a refractory period of τ ref = 2 ms). The neuron model is based on a reduced dimensional integrate-and-fire model previously developed in the literature (Tao et al, 2004 ; Lei et al, 2016 ).…”

Dynamics of sensory integration of olfactory and mechanical stimuli within the response patterns of moth antennal lobe neurons

“…Upon any neuron reaching a threshold voltage of V thres = 1, a spike is recorded and its voltage subsequently reset to V L = 0 (and held at V L = 0 for a refractory period of τ ref = 2ms). The neuron model is based on a reduced dimensional integrate-and-fire model previously developed in the literature (Tao et al, 2004;Lei, Yu, et al, 2016).…”

In-situ recording of ionic currents in projection neurons and Kenyon cells in the olfactory pathway of the honeybee

“…Therefore, it is more likely that ionic currents cause the change in stimulus representation, as shown in the cockroach [ 31 ]. Furthermore, SK channels in Manduca PNs are thought to mediate an after hyperpolarization following pheromone responses [ 48 , 49 ]. Both the N-shaped K Ca currents in cockroaches (31) and the SK channels in Manduca PNs [ 48 , 49 ] are likely to shorten odor responses.…”

“…Furthermore, SK channels in Manduca PNs are thought to mediate an after hyperpolarization following pheromone responses [ 48 , 49 ]. Both the N-shaped K Ca currents in cockroaches (31) and the SK channels in Manduca PNs [ 48 , 49 ] are likely to shorten odor responses. Both the transient and the persistent K + currents we observed in honeybee KCs are relatively large compared to the inward currents and can therefore support the generation of temporally sparse, phasic responses.…”