Purinergic Modulation of Activity in the Developing Auditory Pathway
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REVIEW
Purinergic Modulation of Activity in the Developing Auditory Pathway Sasa Jovanovic1
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Ivan Milenkovic1
Received: 1 April 2020 / Accepted: 10 September 2020 Ó Shanghai Institutes for Biological Sciences, CAS 2020
Abstract Purinergic P2 receptors, activated by endogenous ATP, are prominently expressed on neuronal and nonneuronal cells during development of the auditory periphery and central auditory neurons. In the mature cochlea, extracellular ATP contributes to ion homeostasis, and has a protective function against noise exposure. Here, we focus on the modulation of activity by extracellular ATP during early postnatal development of the lower auditory pathway. In mammals, spontaneous patterned activity is conveyed along afferent auditory pathways before the onset of acoustically evoked signal processing. During this critical developmental period, inner hair cells fire bursts of action potentials that are believed to provide a developmental code for synaptic maturation and refinement of auditory circuits, thereby establishing a precise tonotopic organization. Endogenous ATP-release triggers such patterned activity by raising the extracellular K? concentration and contributes to firing by increasing the excitability of auditory nerve fibers, spiral ganglion neurons, and specific neuron types within the auditory brainstem, through the activation of diverse P2 receptors. We review recent studies that provide new models on the contribution of purinergic signaling to early development of the afferent auditory pathway. Further, we discuss potential future directions of purinergic research in the auditory system. Keywords Purinergic signaling Auditory system Development Cochlea Spiral ganglion Auditory brainstem & Ivan Milenkovic [email protected] 1
School of Medicine and Health Sciences, Carl von Ossietzky University Oldenburg, 26129 Oldenburg, Germany
Introduction In the early 1970s ATP was recognized as a neurotransmitter molecule [1], opening a whole new research field of purinergic transmission and cellular signaling. Numerous studies revealed the importance of purinergic signaling in glial and neuronal communication, under both physiological and pathological conditions [2]. It was postulated that ATP is stored at different concentrations in probably every neuronal synaptic vesicle [3]. Vesicular release of ATP, and its co-release with other neurotransmitters, occur from both neurons and astrocytes [4–11]. Alternatively, ATP can be delivered to the extracellular space via membrane channels, such as connexin hemichannels [12–14], pannexin 1 [15–17], Ca2? homeostasis modulator 1–3 [18–20], volume-regulated anion channels [21, 22], maxi-anion channels [23], and the P2X7 receptor [24]. Once released, extracellular ATP and its breakdown product adenosine exert a wide range of cellular effects by activating plasma membrane-localized receptors. Purinoreceptors were first described in 1976 [25], and thereafter classified into two receptor families: P1 and P
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