Speed and Noise of Neural Membranes: Ion Channel Limitations to Visual Information Transmission

Abstract

In dim light, photoreceptor cells and subsequent neural elements typically show high absolute sensitivity, implying that both phototransduction and synaptic transmission work at a high gain and even a single photon may produce a large electrical response. However, when there is more light, rapid adaptation at several levels of signal processing ensures that the information channel is not congested, but optimally filled with relevant voltage responses. All this is achieved by carefully tuned mechanisms that include several types of ion channels in the cell membrane. These ion-channel mechanisms have been thoroughly investigated in a few species of invertebrates and vertebrates, and some general principles are being revealed. The membrane capacitance and the resistance of the cell together define the time constant of the membrane, thus the maximum speed for building up a voltage response to light. Both in vertebrate cones and in insect microvillar photoreceptors, phototransduction takes place in an enlarged part of the cell membrane, which implies a large capacitance. This can be counteracted by making the membrane more leaky by opening more ion channels. In insect photoreceptors several types of potassium channels have been identified that perform exactly this kind of function. The types of channels vary according to the required speed of phototransduction, ie depending on the life style of the animal. In diurnal dipteran insects the potassium channels are typically of the slowly inactivating type. This channel type regulates the cell impedance according to the depolarisation caused by light stimulation. In insects active in dim environments, the potassium channels found have been predominantly rapidly inactivating. The function of this type of channels is currently under debate. In vertebrate photoreceptors several potassium channel types, including channels sensitive to intracellular calcium and pH, are expressed in the inner segments and modulate photoresponses. Opening and closing of the potassium channels also generates neural noise and thus degrades the signal-to-noise ratio (SNR). However, if the gain of phototransduction is high enough, the dominant noise comes from photon fluctuations, or from the biochemical transduction machinery, or—in some situations—from spontaneous photon-like events. Channel noise is then insignificant by comparison. Thus the optimisation of the SNR is a trade-off between bandwidth (ie speed) and amplification of the signal, and here the voltage-gated potassium channels are of prime importance.