Abstract
In the neonate forebrain, network formation is driven by the spontaneous synchronized activity of pyramidal cells and interneurons, consisting of bursts of electrical activity and intracellular Ca2+ oscillations. By employing ratiometric Na+ imaging in tissue slices obtained from animals at postnatal day 2–4 (P2–4), we found that 20% of pyramidal neurons and 44% of astrocytes in neonatal mouse hippocampus also exhibit transient fluctuations in intracellular Na+. These occurred at very low frequencies (~2/h), were exceptionally long (~8 min), and strongly declined after the first postnatal week. Similar Na+ fluctuations were also observed in the neonate neocortex. In the hippocampus, Na+ elevations in both cell types were diminished when blocking action potential generation with tetrodotoxin. Neuronal Na+ fluctuations were significantly reduced by bicuculline, suggesting the involvement of GABAA-receptors in their generation. Astrocytic signals, by contrast, were neither blocked by inhibition of receptors and/or transporters for different transmitters including GABA and glutamate, nor of various Na+-dependent transporters or Na+-permeable channels. In summary, our results demonstrate for the first time that neonatal astrocytes and neurons display spontaneous ultraslow Na+ fluctuations. While neuronal Na+ signals apparently largely rely on suprathreshold GABAergic excitation, astrocytic Na+ signals, albeit being dependent on neuronal action potentials, appear to have a separate trigger and mechanism, the source of which remains unclear at present.
Highlights
The first week after birth constitutes a time of dynamic rearrangement within the mammalianCNS
Within the observation period of 60 min, fluctuations were present in 43% of recorded astrocytes (n = 92/213 cells; Cells 2020, 9, x spontaneous fluctuations of somatic Na+ in a subset of sulforhodamine 101 (SR101)-positive astrocytes in the CA1 stratum radiatum and in CA1 pyramidal neurons (Figure 1A)
The present study demonstrates for the first time that astrocytes and neurons in neonatal The present study demonstrates for the first time that astrocytes and neurons in neonatal mouse mouse hippocampus and cortex undergo slow, long-lasting fluctuations in their intracellular Na++
Summary
The first week after birth constitutes a time of dynamic rearrangement within the mammalianCNS. Neurogenesis in rodents is mostly completed before birth and the neonatal period is characterized by synchronized, universal activity—which acts to guide the maturation of individual cells and their integration into the complex networks critical to the function of mature tissue [1,2,3]. This activity includes early network oscillations (ENOs) in intracellular calcium (Ca2+ ) [4] and later, the related giant depolarizing potentials (GDPs) of neurons [5]. Glutamatergic excitation takes over at the end of the first postnatal week, and major synaptogenesis and synapse maturation start to surge in the 2nd and 3rd week after birth [7,8]
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