Common dynamical features of sensory adaptation in photoreceptors and olfactory sensory neurons

Palo, Giovanna De; Facchetti, Giuseppe; Mazzolini, Monica; Menini, Anna; Torre, Vincent; Altafini, Claudio

doi:10.1038/srep01251

Cited by 36 publications

(53 citation statements)

References 46 publications

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“…24, 25 Similarly, in the cardiovascular system, it has been previously shown that sympathetic nerve activity measured by muscle sympathetic nerve activity was greater when the heart was paced irregularly, and these findings were independent of hemodynamic changes. 26 We speculate that variability of PVC CI compared to fixed CI may prevent neural adaptation and play an important role in reflex activation of the ANS.…”

Section: Discussionmentioning

confidence: 90%

Premature Ventricular Contraction Coupling Interval Variability Destabilizes Cardiac Neuronal and Electrophysiological Control

Hamon¹,

Rajendran²,

Chui³

et al. 2017

Circ: Arrhythmia and Electrophysiology

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Background Variability in premature ventricular contraction (PVC) coupling interval (CI) increases the risk of cardiomyopathy and sudden death. The autonomic nervous system regulates cardiac electrical and mechanical indices, and its dysregulation plays an important role in cardiac disease pathogenesis. The impact of PVCs on the intrinsic cardiac nervous system (ICNS), a neural network on the heart, remains unknown. The objective was to determine the effect of PVCs and CI on ICNS function in generating cardiac neuronal and electrical instability using a novel cardio-neural mapping approach. Methods and Results In a porcine model (n=8) neuronal activity was recorded from a ventricular ganglion using a microelectrode array, and cardiac electrophysiological mapping was performed. Neurons were functionally classified based on their response to afferent and efferent cardiovascular stimuli, with neurons that responded to both defined as convergent (local reflex processors). Dynamic changes in neuronal activity were then evaluated in response to right ventricular outflow tract PVCs with fixed short, fixed long, and variable CI. PVC delivery elicited a greater neuronal response than all other stimuli (P<0.001). Compared to fixed short and long CI, PVCs with variable CI had a greater impact on neuronal response (P<0.05 versus short CI), particularly on convergent neurons (P<0.05), as well as neurons receiving sympathetic (P<0.05) and parasympathetic input (P<0.05). The greatest cardiac electrical instability was also observed following variable (short) CI PVCs. Conclusions Variable CI PVCs affect critical populations of ICNS neurons and alter cardiac repolarization. These changes may be critical for arrhythmogenesis and remodeling leading to cardiomyopathy.

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Section: Discussionmentioning

confidence: 90%

Premature Ventricular Contraction Coupling Interval Variability Destabilizes Cardiac Neuronal and Electrophysiological Control

Hamon¹,

Rajendran²,

Chui³

et al. 2017

Circ: Arrhythmia and Electrophysiology

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“…Similarly to Drosophila Or-expressing OSNs, sensory neurons in many other modalities, such as hair cells (49) adaptation in other senses. With respect to modeling, it remains a challenge to understand the general effects of adaptation according to the underlying molecular mechanisms in sensory neurons (50), as has been done in the simpler case of bacterial chemotaxis (51). The ability of strong adaptation by Ors would allow Drosophila to track odor changes over a broad range of concentrations and to detect other odors even in the presence of certain background odor.…”

Section: Discussionmentioning

confidence: 99%

Distinct signaling of Drosophila chemoreceptors in olfactory sensory neurons

Cao

Jing

Yang

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

114

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In Drosophila, olfactory sensory neurons (OSNs) rely primarily on two types of chemoreceptors, odorant receptors (Ors) and ionotropic receptors (Irs), to convert odor stimuli into neural activity. The cellular signaling of these receptors in their native OSNs remains unclear because of the difficulty of obtaining intracellular recordings from Drosophila OSNs. Here, we developed an antennal preparation that enabled the first recordings (to our knowledge) from targeted Drosophila OSNs through a patch-clamp technique. We found that brief odor pulses triggered graded inward receptor currents with distinct response kinetics and current-voltage relationships between Or-and Ir-driven responses. When stimulated with long-step odors, the receptor current of Ir-expressing OSNs did not adapt. In contrast, Or-expressing OSNs showed a strong Ca 2+ -dependent adaptation. The adaptation-induced changes in odor sensitivity obeyed the Weber-Fechner relation; however, surprisingly, the incremental sensitivity was reduced at low odor backgrounds but increased at high odor backgrounds. Our model for odor adaptation revealed two opposing effects of adaptation, desensitization and prevention of saturation, in dynamically adjusting odor sensitivity and extending the sensory operating range.Drosophila | olfaction | chemoreceptor | sensory adaptation | OSN

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“…Dissociated rods were obtained from adult male Xenopus laevis frogs (Xenopus express, Ancienne Ecole de Vernassal, Le Bourg, France) as previously reported (62,63). OS lengths for green-sensitive and blue-sensitive rods (64) where 31 ± 1 μm (n = 85) and 26 ± 1.5 μm (n = 17), respectively, and the OS diameter is about 4-6 μm.…”

Section: Methodsmentioning

confidence: 99%

The phototransduction machinery in the rod outer segment has a strong efficacy gradient

Mazzolini

Facchetti

Andolfi

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Rod photoreceptors consist of an outer segment (OS) and an inner segment. Inside the OS a biochemical machinery transforms the rhodopsin photoisomerization into electrical signal. This machinery has been treated as and is thought to be homogenous with marginal inhomogeneities. To verify this assumption, we developed a methodology based on special tapered optical fibers (TOFs) to deliver highly localized light stimulations. By using these TOFs, specific regions of the rod OS could be stimulated with spots of light highly confined in space. As the TOF is moved from the OS base toward its tip, the amplitude of saturating and single photon responses decreases, demonstrating that the efficacy of the transduction machinery is not uniform and is 5-10 times higher at the base than at the tip. This gradient of efficacy of the transduction machinery is attributed to a progressive depletion of the phosphodiesterase along the rod OS. Moreover we demonstrate that, using restricted spots of light, the duration of the photoresponse along the OS does not increase linearly with the light intensity as with diffuse light.V ertebrate photoreceptors, rods and cones, are morphologically specialized light sensing neurons and consist of four parts: an outer segment (OS), an inner segment (IS), the nuclear region, and the synapse (1). The OS of rod photoreceptors is stacked with thousands of lipid discs containing rhodopsin molecules that absorb photons (2-4). They are surrounded by a plasma membrane and differ in their lipid and protein composition.It is known that within 1 s, each excited rhodopsin, densely packed in the disc membrane, activates tens of G proteins (named transducin), each of which activates one phosphodiesterase (PDE) molecule (5-7). Activated PDEs rapidly hydrolyze cytoplasmic cyclic guanosine monophosphate (cGMP) thereby closing cyclic nucleotide-gated (CNG) channels (8, 9). In darkness, a current carried by Na + , K + , and Ca 2+ ions, which is known as the photocurrent, enters via the CNG channels into the OS and is pumped out by Na + /K + ATPase, located in the IS (1). This current can be recorded using suction electrodes (3, 10).The existence of distinct compartments on photoreceptor OSs is a consequence of their function. The OS is a highly modified nonmotile cilium developed for the absorption of light that is translated into the electrical signal. The IS and the nuclear region-containing the organelles and the nucleus-are dedicated to metabolism, homeostasis, and synthesis of the membrane and transportation of proteins and lipids supplied to the OS by an extensive trafficking through the tight restriction connecting the OS to the IS (11). Considering that, unlike typical cilia, the OS is continuously renewed throughout its entire life and given the varying density and asymmetry of the molecules involved, it is not surprising to find an efficacy gradient of phototransduction between the base and the tip. Indeed, the cholesterol (12, 13), the phospholipids (13-15), the CNG channels, the PDE (16), and the rhodop...

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Common dynamical features of sensory adaptation in photoreceptors and olfactory sensory neurons

Cited by 36 publications

References 46 publications

Premature Ventricular Contraction Coupling Interval Variability Destabilizes Cardiac Neuronal and Electrophysiological Control

Premature Ventricular Contraction Coupling Interval Variability Destabilizes Cardiac Neuronal and Electrophysiological Control

Distinct signaling of Drosophila chemoreceptors in olfactory sensory neurons

The phototransduction machinery in the rod outer segment has a strong efficacy gradient

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