Abstract
Cumulative evidence supports bidirectional interactions between astrocytes and neurons, suggesting glial involvement of neuronal information processing in the brain. Cytosolic calcium (Ca2+) concentration is important for astrocytes as Ca2+ surges co-occur with gliotransmission and neurotransmitter reception. Cerebral cortex is organized in layers which are characterized by distinct cytoarchitecture. We asked if astrocyte-dominant layer 1 (L1) of the somatosensory cortex was different from layer 2/3 (L2/3) in spontaneous astrocytic Ca2+ activity and if it was influenced by background neural activity. Using a two-photon laser scanning microscope, we compared spontaneous Ca2+ activity of astrocytic somata and processes in L1 and L2/3 of anesthetized mature rat somatosensory cortex. We also assessed the contribution of background neural activity to the spontaneous astrocytic Ca2+ dynamics by investigating two distinct EEG states (“synchronized” vs. “de-synchronized” states). We found that astrocytes in L1 had nearly twice higher Ca2+ activity than L2/3. Furthermore, Ca2+ fluctuations of processes within an astrocyte were independent in L1 while those in L2/3 were synchronous. Pharmacological blockades of metabotropic receptors for glutamate, ATP, and acetylcholine, as well as suppression of action potentials did not have a significant effect on the spontaneous somatic Ca2+ activity. These results suggest that spontaneous astrocytic Ca2+ surges occurred in large part intrinsically, rather than neural activity-driven. Our findings propose a new functional segregation of layer 1 and 2/3 that is defined by autonomous astrocytic activity.
Highlights
Astrocytes occupy a significant proportion of the cellular composition in the brain
We investigated spontaneously occurring astrocytic calcium (Ca2+) surges in layer 1 (L1) and layer 2/3 (L2/3) of the somatosensory cortex of adult (.P25) rats in vivo in the absence of sensory input
We found there were twice as many ‘‘active astrocytes’’ in L1 than L2/3
Summary
Astrocytes occupy a significant proportion of the cellular composition in the brain. Their functions have been considered to be logistic support for neurons, such as mediating energy metabolism for neurons or maintenance of extracellular medium concentrations [1,2]. While the traditional roles of astrocytes have gained experimental support, evidence has accumulated to suggest bidirectional neuron-glia communications [3] and possible participation in neural information processing [4,5]. The neural activity driven astrocytic Ca2+ surge is triggered by activation of metabotropic neurotransmitter receptors, which leads to production of inositol 1,4,5-triphosphate (IP3), and thereby to release of Ca2+ from the endoplasmic reticulum (ER) [3]. Evidence suggesting a dynamic role of astrocytes through the Ca2+ activity is accumulating in in vitro experiments, an oftexpressed concern is the modification of cellular properties of astrocytes due to the invasive nature of the preparations [12]
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