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

Abstract

14Brains processes information through the coordinated efforts of billions of individual neurons, each 15 encoding a small part of the overall information stream. Central to this is how neurons integrate and 16 transform complex patterns of synaptic inputs. The neuronal membrane impedance sets the gain and 17 timing for synaptic integration, determining a neuron's ability to discriminate between synaptic input 18 patterns. Using single and dual dendritic recordings in vivo, pharmacology, and computational 19 morphologies, including those of neocortical pyramidal neurons and cerebellar Purkinje cells. These 30 findings further our understanding of the integration properties of individual neurons by showing the 31 unexpected role played by two widespread active conductances and by dendritic morphology in 32 shaping synaptic integration. 33 New & Noteworthy 34Neuronal integration depends on complex interactions between synaptic input patterns and the 35 electrochemical properties of dendrites. We used an identified collision detection neuron in 36 grasshoppers to examine how its morphology and two membrane conductances determine the gain and 37 timing of synaptic integration in relation to the computations it performs. The neuronal properties 38 examined are ubiquitous and therefore further a general understanding of neuronal computations, 39 including those in our own brain. 40Keywords: dendritic processing, collision avoidance, impedance, lobula giant movement detector 41 channels (Dewell and Gabbiani 2018a, 2018b; Gabbiani et al. 2002; Peron and Gabbiani 2009). 78 Different aspects of the LGMD's firing patterns -including burst firing -have been tied to the 79 generation of escape behaviors (Dewell and Gabbiani 2018a; Fotowat et al. 2011; McMillan and Gray 80 2015). Currently, no one has characterized the LGMD's membrane impedance to determine how it 81 shapes this neuron's dendritic integration and visual computations. 82Neuronal membrane properties have mainly been studied with cultured neurons or brain slices 83 and the natural synaptic input patterns are still unknown for most neurons, so much remains 84 unanswered about how the impedance properties of neurons influence synaptic integration and neural 85 computations in vivo. As both gH and gM are sensitive to numerous modulators (Delmas and Brown 86 2005; Wahl-Schott and Biel 2009), our ability to conduct experiments in vivo ensures that the channels 87 are in the relevant modulatory state. We discovered that the LGMD membrane impedance is broadband 88 and generates small delays between synaptic current and membrane potential that remain consistent 89 across membrane potentials. The HCN and M channels, their interactions, and the neuronal 90 morphology all contribute to producing this broadband impedance profile which increases the LGMD's 91 ability to discriminate behaviorally relevant patterns of synaptic inputs from irrelevant ones. 92 Materials and Methods 93 Animals 94Experiments were performed on adult female grasshoppers 7-12 weeks of age (Schistoc...