Laboratory of Comparative Sensory Physiology, Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, Saint Petersburg, Russia.
PLoS One. 2023 Aug 1;18(8):e0289466. doi: 10.1371/journal.pone.0289466. eCollection 2023.
Evolution produced a large variety of rhabdomeric photoreceptors in the compound eyes of insects. To study effects of morphological and electrophysiological differences on signal generation and modulation, we developed models of the cockroach and blow fly photoreceptors. The cockroach model included wide microvilli, large membrane capacitance and two voltage-activated K+ conductances. The blow fly model included narrow microvilli, small capacitance and two sustained voltage-activated K+ conductances. Our analysis indicated that membrane of even the narrowest microvilli of up to 3 μm long can be measured fully from the soma. Attenuation of microvillar quantum bump (QB)-like signals at the recording site in the soma increased with the signal amplitude in the microvillus, due to the decreasing driving force. However, conductance of the normal-sized QBs can be detected in the soma with minimal attenuation. Next, we investigated how interactions between the sustained voltage-activated K+ and light-induced conductances can shape the frequency response. The models were depolarized by either a current injection or light-induced current (LIC) and probed with inward currents kinetically approximating dark- or light-adapted QBs. By analyzing the resulting voltage impulse responses (IR), we found that: (1) sustained K+ conductance can shorten IRs, expanding the signaling bandwidth beyond that set by phototransduction; (2) voltage-dependencies of changes in IR durations have minima within the physiological voltage response range, depending on the activation kinetics of K+ conductance, the presence or absence of sustained LIC, and the kinetics of the probing current stimulus; and (3) sustained LIC lowers gain of IRs and can exert dissimilar effects on their durations. The first two findings were supported by experiments. It is argued that improvement of membrane response bandwidth by parametric interactions between passive, ligand-gated and voltage-dependent components of the membrane circuit can be a general feature of excitable cells that respond with graded voltage signals.
昆虫复眼的光感受器经历了漫长的进化，产生了多种多样的结构。为了研究形态和电生理差异对信号产生和调制的影响，我们构建了蟑螂和果蝇光感受器模型。蟑螂模型的光感受器具有宽大的微绒毛、较大的膜电容和两种电压激活的 K+ 电导；果蝇模型的光感受器具有狭窄的微绒毛、较小的电容和两种持续激活的电压激活的 K+ 电导。我们的分析表明，即使是长达 3μm 的最窄微绒毛的膜电位也可以从胞体上完全测量到。由于驱动力的减小，在胞体记录部位微绒毛量子斑（QB）样信号的衰减随着微绒毛中信号幅度的增加而增加。然而，正常大小的 QB 电导可以在胞体中以最小的衰减检测到。接下来，我们研究了持续激活的 K+电导和光诱导电流（LIC）之间的相互作用如何影响频率响应。模型通过电流注入或光诱导电流（LIC）去极化，并通过与暗适应或光适应 QB 动力学上相似的内向电流进行探测。通过分析产生的电压脉冲响应（IR），我们发现：（1）持续的 K+电导可以缩短 IR，将信号带宽扩展到光感受器之外；（2）IR 持续时间的电压依赖性在生理电压响应范围内具有最小值，这取决于 K+电导的激活动力学、持续 LIC 的存在与否，以及探测电流刺激的动力学；（3）持续的 LIC 降低了 IR 的增益，并对其持续时间产生不同的影响。前两个发现得到了实验的支持。我们认为，通过膜电路中被动、配体门控和电压依赖组件之间的参数相互作用来改善膜响应带宽，可以作为具有分级电压信号响应的可兴奋细胞的一个普遍特征。
