Abstract
The retina and the olfactory bulb are the gateways to the visual and olfactory systems, respectively, similarly using neural networks to initiate sensory signal processing. Sensory receptors receive signals that are transmitted to neural networks before projecting to primary cortices. These networks filter sensory signals based on their unique features and adjust their sensitivities by gain control systems. Interestingly, dopamine modulates sensory signal transduction in both systems. In the retina, dopamine adjusts the retinal network for daylight conditions (“light adaptation”). In the olfactory system, dopamine mediates lateral inhibition between the glomeruli, resulting in odorant signal decorrelation and discrimination. While dopamine is essential for signal discrimination in the olfactory system, it is not understood whether dopamine has similar roles in visual signal processing in the retina. To elucidate dopaminergic effects on visual processing, we conducted patch-clamp recording from second-order retinal bipolar cells, which exhibit multiple types that can convey different temporal features of light. We recorded excitatory postsynaptic potentials (EPSPs) evoked by various frequencies of sinusoidal light in the absence and presence of a dopamine receptor 1 (D1R) agonist or antagonist. Application of a D1R agonist, SKF-38393, shifted the peak temporal responses toward higher frequencies in a subset of bipolar cells. In contrast, a D1R antagonist, SCH-23390, reversed the effects of SKF on these types of bipolar cells. To examine the mechanism of dopaminergic modulation, we recorded voltage-gated currents, hyperpolarization-activated cyclic nucleotide-gated (HCN) channels, and low-voltage activated (LVA) Ca2+ channels. SKF modulated HCN and LVA currents, suggesting that these channels are the target of D1R signaling to modulate visual signaling in these bipolar cells. Taken together, we found that dopamine modulates the temporal tuning of a subset of retinal bipolar cells. Consequently, we determined that dopamine plays a role in visual signal processing, which is similar to its role in signal decorrelation in the olfactory bulb.
Highlights
Continuous integration of our sensory perceptions gives rise to our daily experience of the world, and this experience is made possible by specialized neuronal ‘‘antennae,’’ such as the retina and the olfactory bulb
L-excitatory postsynaptic potentials (EPSPs) for individual cells were analyzed by Fourier Transformation (FFT) (Figure 1), which revealed the frequencies of sinewave stimuli and light-evoked excitatory postsynaptic potentials (L-EPSPs) amplitudes for those frequencies
Using retinal slice preparations from the mouse, we examined the effect of a D1R agonist and antagonist on the temporal features of bipolar cell signaling
Summary
Continuous integration of our sensory perceptions gives rise to our daily experience of the world, and this experience is made possible by specialized neuronal ‘‘antennae,’’ such as the retina and the olfactory bulb. The retina and the olfactory bulb utilize similar neural network architecture despite processing different signals. In both systems, sensory signals stimulate sensory. Second-order neurons, bipolar cells, converge photoreceptor input, and begin the process of extracting abstract visual features such as luminance, contrast, chromaticity, and spatiotemporal properties of light signals. This information is modulated by horizontal and amacrine cells and relayed to third-order retinal ganglion cells (RGCs), the output neurons of the retina (Wässle, 2004; Dowling, 2012). In the olfactory system, olfactory receptor neurons (ORNs) in the nasal cavity convey odorant signals to the glomeruli structures in the olfactory bulb, where signals are modulated by juxtaglomerular cells before being sent out to the olfactory cortex by the olfactory output neurons, mitral and tufted cells (Astic et al, 1987; Stewart and Pedersen, 1987; Ressler et al, 1994; Gire et al, 2012)
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