M current regulates firing mode and spike reliability in a collision-detecting neuron

Abstract

All animals must detect impending collisions to escape and reliably discriminate them from nonthreatening stimuli, thus preventing false alarms. Therefore, it is no surprise that animals have evolved highly selective and sensitive neurons dedicated to such tasks. We examined a well-studied collision-detection neuron in the grasshopper ( Schistocerca americana) using in vivo electrophysiology, pharmacology, and computational modeling. This lobula giant movement detector (LGMD) neuron is excitable by inputs originating from each ommatidia of the compound eye. It possesses many intrinsic properties that increase its selectivity to objects approaching on a collision course, including switching between burst and nonburst firing. In this study, we demonstrate that the LGMD neuron exhibits a large M current, generated by noninactivating K channels, that shortens the temporal window of dendritic integration, regulates a firing mode switch between burst and isolated spiking, increases the precision of spike timing, and increases the reliability of spike propagation to downstream motor centers. By revealing how the M current increases the LGMD's ability to detect impending collisions, our results suggest that similar channels may play an analogous role in other collision detection circuits. NEW & NOTEWORTHY The ability to reliably detect impending collisions is a critical survival skill. The nervous systems of many animals have developed dedicated neurons for accomplishing this task. We used a mix of in vivo electrophysiology and computational modeling to investigate the role of M potassium channels within one such collision-detecting neuron and show that through regulation of burst firing and enhancement of spiking reliability, the M current increases the ability to detect impending collisions.

Active membrane conductances and morphology of a collision detection neuron broaden its impedance profile and improve membrane synchrony

“…The LGMD also has a CaLVA conductance that can generate 654 bursting (Peron and Gabbiani, 2009;Dewell and Gabbiani, 2018b). As recently shown, gM antagonizes 655 this bursting, thus regulating the LGMD firing pattern (Dewell and Gabbiani, 2018b). Blockade of gM 656 also generated a change in impedance amplitude resulting in a 2-5 Hz resonance (Fig.…”

“…Blockade of gM 656 also generated a change in impedance amplitude resulting in a 2-5 Hz resonance (Fig. 5D) matching 657 the frequency range of LGMD calcium bursts following gM block (Dewell and Gabbiani, 2018b). In 658 hippocampal pyramidal neurons gM blockade does not result in resonance (Hu et al, 2002(Hu et al, , 2009, 659 suggesting that gM antagonism of a CaLVA conductance likely does not occur in these neurons.…”

“…This increased 4 Hz impedance likely helps generate the increased spiking observed in response to ~4 492 Hz inputs following gM blockade (Dewell & Gabbiani 2018b). After gM blockade the impedance phase 493 increased at frequencies ≤ 2 Hz and decreased at higher frequencies (Fig.…”

“…In thalamic relay 652 neurons, low voltage activated Ca 2+ (CaLVA) channels produce bursting and a 2-4 Hz resonance 653 (Hutcheon et al, 1994;Puil et al, 1994). The LGMD also has a CaLVA conductance that can generate 654 bursting (Peron and Gabbiani, 2009;Dewell and Gabbiani, 2018b). As recently shown, gM antagonizes 655 this bursting, thus regulating the LGMD firing pattern (Dewell and Gabbiani, 2018b).…”

“…LGMD subthreshold membrane potential exhibited zero phase and hence was most synchronous at ~1 438 Hz, in contrast to spiking which is most synchronous at 6 Hz (Dewell & Gabbiani 2018b). 439…”