Biomedical subjects
Publications and source records attributed to Jeremy E Niven.
Tracking moving targets is essential for animals that pursue prey or conspecifics. Recent studies in male and female hoverflies have described classes of neurons that detect the movements of small targets against a moving background but the mechanisms generating their responses remain unclear.
Determining the contribution of a single type of ion channel to information processing within a neuron requires not only knowledge of the properties of the channel but also understanding of its function within a complex system. We studied the contribution of slow delayed rectifier K+ channels to neural coding in Drosophila photoreceptors by combining genetic and electrophysiological approaches with biophysical modeling. We show that the Shab gene encodes the slow delayed rectifier K+ channel and identify a novel voltage-gated K+ conductance. Analysis of the in vivo recorded voltage responses together with their computer-simulated counterparts demonstrates that Shab channels in Drosophila photoreceptors attenuate the light-induced depolarization and prevent response saturation in bright light. We also show that reduction of the Shab conductance in mutant photoreceptors is accompanied by a proportional drop in their input resistance. This reduction in input resistance partially restores the signaling range, sensitivity, and dynamic coding of light intensities of Shab photoreceptors to those of the wild-type counterparts. However, loss of the Shab channels may affect both the energy efficiency of coding and the processing of natural stimuli. Our results highlight the role of different types of voltage-gated K+ channels in the performance of the photoreceptors and provide insight into functional robustness against the perturbation of specific ion channel composition.
Recent studies on bats, goats and hominids suggest that some mammalian brains may have undergone dramatic evolutionary reductions in size. These studies emphasise the importance of selective pressures upon mammalian brain evolution and the need to integrate studies of neuroanatomy, neurophysiology and behaviour.
Voltage-gated K(+) channels are important in neuronal signaling, but little is known of their interactions with receptor currents or their behavior during natural stimulation. We used nonparametric and parametric nonlinear modeling of experimental responses, combined with Hodgkin-Huxley style simulation, to examine the roles of K(+) channels in forming the responses of wild-type (WT) and Shaker mutant (Sh(14)) Drosophila photoreceptors to naturalistic stimulus sequences. Naturalistic stimuli gave results different from those of similar experiments with white noise stimuli. Sh(14) responses were larger and faster than WT. Simulation indicated that, in addition to eliminating the Shaker current, the mutation changed the current flowing through light-dependent channels [light-induced current (LIC)] and increased the delayed rectifier current. Part of the change in LIC could be attributed to direct feedback from the voltage-sensitive ion channels to the light-sensitive channels by the membrane potential. However, we argue that other changes occur in the light detecting machinery of Sh(14) mutants, possibly during photoreceptor development.
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We describe the contribution of rapidly inactivating Shaker K+ channels to the dynamic membrane properties of Drosophila photoreceptors. Phototransduction was measured in wild-type and Shaker mutant (Sh14) Drosophila photoreceptors by stimulating with white noise-modulated light contrast and recording the resulting intracellular membrane potential fluctuations. A second-order Volterra kernel series was used to characterize the nonlinear dynamic properties of transduction in the two situations. First-order kernels were indistinguishable in wild-type and Sh14 photoreceptors, indicating that the basic light transduction machinery was always intact. However, second-order kernels of Shaker mutants lacked a large, early amplification, indicating a novel role for Shaker K+ channels in amplifying and accelerating the voltage response of wild-type photoreceptors. A cascade model of two nonlinear static components surrounding one linear dynamic component was able to partially reproduce the experimental responses. Parameters obtained by fitting the model to the experimental data supported the hypothesis that normal Shaker K+ channels contribute an early, positive nonlinearity that partially offsets a later attenuating nonlinearity caused by membrane shunting.
An array of rapidly inactivating voltage-gated K+ channels is distributed throughout the nervous systems of vertebrates and invertebrates. Although these channels are thought to regulate the excitability of neurons by attenuating voltage signals, their specific functions are often poorly understood. We studied the role of the prototypical inactivating K+ conductance, Shaker, in Drosophila photoreceptors by recording intracellularly from wild-type and Shaker mutant photoreceptors. Here we show that loss of the Shaker K+ conductance produces a marked reduction in the signal-to-noise ratio of photoreceptors, generating a 50% decrease in the information capacity of these cells in fully light-adapted conditions. By combining experiments with modelling, we show that the inactivation of Shaker K+ channels amplifies voltage signals and enables photoreceptors to use their voltage range more effectively. Loss of the Shaker conductance attenuated the voltage signal and induced a compensatory decrease in impedance. Our results demonstrate the importance of the Shaker K+ conductance for neural coding precision and as a mechanism for selectively amplifying graded signals in neurons, and highlight the effect of compensatory mechanisms on neuronal information processing.