Action Potential Activity and Membrane Structure in Neurons of the Goldfish Retina Undergo Seasonal Changes

Abstract

Seasonal changes in the structure of cell membranes may occur as an adaptive measure to withstand exposure to prolonged, environmental stress. Little is known, however, about how such biophysical changes may impact sensory systems and other aspects of the CNS in vertebrates. We compared membrane properties of neurons from the retina of goldfish (Carassius auratus), an organism well-suited to environmental change, during the summer and winter months. We isolated horizontal cells, which modulate output from light-sensitive photoreceptors in the retina and display spontaneous Ca2+-based action potentials in vitro and in situ. Measurement of intracellular Ca2+ concentration using Fura-2 microspectrofluorometry demonstrated that action potentials were of lower frequency and higher amplitude in cells isolated from goldfish during the winter months. Analysis of action potential activity using current-clamp electrophysiology correlated changes in frequency and amplitude with resting membrane potential, such that membrane hyperpolarization gave rise to a winter phenotype. Indeed, voltage-clamp recording of horizontal cells isolated during the winter confirmed that neurons displayed a resting membrane potential that was hyperpolarized by approximately 20 mV, compared to summer neurons, suggestive of a seasonal effect on membrane excitability. Analysis of whole-retina phospholipid composition using mass spectrometry revealed a significant change in membrane structure during the winter, including a 2-fold increase in phosphatidylethanolamine species. These studies indicate significant biophysical modification that occurs in retinal neurons of goldfish throughout the year, and suggests profound seasonal variation in visual processing and CNS physiology in organisms adapted to survive environmental change.