Changes in electrophysiological properties of photoreceptors in Periplaneta americana associated with the loss of screening pigment

J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2018 Nov;204(11):915-928. doi: 10.1007/s00359-018-1290-0. Epub 2018 Sep 20.

Abstract

Absence of screening pigment in insect compound eyes has been linked to visual dysfunction. We investigated how its loss in a white-eyed mutant (W-E) alters the photoreceptor electrophysiological properties, opsin gene expression, and the behavior of the cockroach, Periplaneta americana. Whole-cell patch-clamp recordings of green-sensitive photoreceptors in W-E cockroaches gave reduced membrane capacitance, absolute sensitivity to light, and light-induced currents. Decreased low-pass filtering increased voltage-bump amplitudes in W-E photoreceptors. Intracellular recordings showed that angular sensitivity of W-E photoreceptors had two distinct components: a large narrow component with the same acceptance angle as wild type, plus a relatively small wide component. Information processing was evaluated using Gaussian white-noise modulated light stimulation. In bright light, W-E photoreceptors demonstrated higher signal gain and signal power than wild-type photoreceptors. Expression levels of the primary UV- and green-sensitive opsins were lower and the secondary green-sensitive opsin significantly higher in W-E than in wild-type retinae. In behavioral experiments, W-E cockroaches were significantly less active in dim green light, consistent with the relatively low light sensitivity of their photoreceptors. Overall, these differences can be related to the loss of screening pigment function and to a compensatory decrease in the rhabdomere size in W-E retinae.

Keywords: Compound eye; Periplaneta americana; Photoreceptor; Screening pigment; White-eyed.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Behavior, Animal / physiology
  • Compound Eye, Arthropod / physiology*
  • Electric Capacitance
  • Gene Expression
  • Insect Proteins / metabolism
  • Intracellular Space / physiology
  • Male
  • Membrane Potentials / physiology
  • Motor Activity
  • Opsins / metabolism
  • Patch-Clamp Techniques
  • Periplaneta / physiology*
  • Photic Stimulation
  • Photoreceptor Cells, Invertebrate / physiology*
  • Pigmentation
  • Potassium / metabolism
  • RNA, Messenger / metabolism
  • Signal Transduction / physiology
  • Vision, Ocular / physiology*

Substances

  • Insect Proteins
  • Opsins
  • RNA, Messenger
  • Potassium