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PLOS ONE  2008 

Cortical Layer 1 and Layer 2/3 Astrocytes Exhibit Distinct Calcium Dynamics In Vivo

DOI: 10.1371/journal.pone.0002525

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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.

References

[1]  Nedergaard M, Ransom B, Goldman SA (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 26: 523–530.
[2]  Verkhratsky A, Butt A (2007) Glial Neurobiology. Hoboken, NJ: Wiley.
[3]  Perea G, Araque A (2005) Glial calcium signaling and neuron-glia communication. Cell Calcium 38: 375–382.
[4]  Deitmer JW, McCarthy KD, Scemes E, Giaume C (2006) Information processing and transmission in glia: calcium signaling and transmitter release. Glia 54: 639–641.
[5]  Moller C, Lucke J, Zhu J, Faustmann PM, Malsburg Cvd (2007) Glial cells for information routing? Cognitive Systems Research 8: 28–35.
[6]  Perea G, Araque A (2007) Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317: 1083–1086.
[7]  Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, et al. (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310: 113–116.
[8]  Porter JT, McCarthy KD (1997) Astrocytic neurotransmitter receptors in situ and in vivo. Prog Neurobiol 51: 439–455.
[9]  Fiacco TA, McCarthy KD (2006) Astrocyte calcium elevations: properties, propagation, and effects on brain signaling. Glia 54: 676–690.
[10]  Fiacco TA, Agulhon C, Taves SR, Petravicz J, Casper KB, et al. (2007) Selective stimulation of astrocyte calcium in situ does not affect neuronal excitatory synaptic activity. Neuron 54: 611–626.
[11]  Nett WJ, Oloff SH, McCarthy KD (2002) Hippocampal astrocytes in situ exhibit calcium oscillations that occur independent of neuronal activity. J Neurophysiol 87: 528–537.
[12]  Kudo Y, Takita M, Nakamura K, Sugaya K, Ogura A (1993) Heterogeneous Distribution of Functional Glutamate Receptor Subtypes in Organotypic Slice Culture of Rat Hippocampus Revealed by Calcium Fluorometry. Bioimages 1: 159–166.
[13]  DeFelipe J, Alonso-Nanclares L, Arellano JI (2002) Microstructure of the neocortex: comparative aspects. J Neurocytol 31: 299–316.
[14]  Steriade M (1997) Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance. Cereb Cortex 7: 583–604.
[15]  Steriade M, Nunez A, Amzica F (1993) A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci 13: 3252–3265.
[16]  Wang X, Lou N, Xu Q, Tian GF, Peng WG, et al. (2006) Astrocytic Ca2+ signaling evoked by sensory stimulation in vivo. Nat Neurosci 9: 816–823.
[17]  Dombeck DA, Khabbaz AN, Collman F, Adelman TL, Tank DW (2007) Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 56: 43–57.
[18]  Hirase H, Qian L, Bartho P, Buzsaki G (2004) Calcium dynamics of cortical astrocytic networks in vivo. PLoS Biol 2: E96.
[19]  Ding S, Fellin T, Zhu Y, Lee SY, Auberson YP, et al. (2007) Enhanced astrocytic Ca2+ signals contribute to neuronal excitotoxicity after status epilepticus. J Neurosci 27: 10674–10684.
[20]  Stosiek C, Garaschuk O, Holthoff K, Konnerth A (2003) In vivo two-photon calcium imaging of neuronal networks. Proc Natl Acad Sci U S A 100: 7319–7324.
[21]  Nimmerjahn A, Kirchhoff F, Kerr JN, Helmchen F (2004) Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat Methods 1: 31–37.
[22]  Takano T, Tian GF, Peng W, Lou N, Libionka W, et al. (2006) Astrocyte-mediated control of cerebral blood flow. Nat Neurosci 9: 260–267.
[23]  Xu HT, Pan F, Yang G, Gan WB (2007) Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex. Nat Neurosci 10: 549–551.
[24]  Amzica F, Steriade M (1995) Short- and long-range neuronal synchronization of the slow (< 1 Hz) cortical oscillation. J Neurophysiol 73: 20–38.
[25]  Mechawar N, Cozzari C, Descarries L (2000) Cholinergic innervation in adult rat cerebral cortex: a quantitative immunocytochemical description. J Comp Neurol 428: 305–318.
[26]  Binns KE, Salt TE (2001) Actions of the systemically active metabotropic glutamate antagonist MPEP on sensory responses of thalamic neurones. Neuropharmacology 40: 639–644.
[27]  Bakin JS, Weinberger NM (1996) Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc Natl Acad Sci U S A 93: 11219–11224.
[28]  Zur Nieden R, Deitmer JW (2006) The role of metabotropic glutamate receptors for the generation of calcium oscillations in rat hippocampal astrocytes in situ. Cereb Cortex 16: 676–687.
[29]  Paxinos G, Franklin KBJ (2001) The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press.
[30]  Majewska AK, Newton JR, Sur M (2006) Remodeling of synaptic structure in sensory cortical areas in vivo. J Neurosci 26: 3021–3029.
[31]  Aguado F, Espinosa-Parrilla JF, Carmona MA, Soriano E (2002) Neuronal activity regulates correlated network properties of spontaneous calcium transients in astrocytes in situ. J Neurosci 22: 9430–9444.
[32]  Yuste R, Nelson DA, Rubin WW, Katz LC (1995) Neuronal domains in developing neocortex: mechanisms of coactivation. Neuron 14: 7–17.
[33]  Schipke CG, Heidemann A, Skupin A, Peters O, Falcke M, et al. (2008) Temperature and nitric oxide control spontaneous calcium transients in astrocytes. Cell Calcium 43: 285–295.
[34]  Fleischhauer K, Vossel A (1979) Cell densities in the various layers of the rabbit's striate area. Anat Embryol (Berl) 156: 269–281.
[35]  Mishima T, Sakatani S, Hirase H (2007) Intracellular Labeling of Single Cortical Astrocytes In Vivo. Journal of Neuroscience Methods 166: 32–40.
[36]  Amzica F, Neckelmann D (1999) Membrane capacitance of cortical neurons and glia during sleep oscillations and spike-wave seizures. J Neurophysiol 82: 2731–2746.
[37]  Seigneur J, Kroeger D, Nita DA, Amzica F (2006) Cholinergic action on cortical glial cells in vivo. Cereb Cortex 16: 655–668.
[38]  Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6: 626–640.
[39]  Sharma G, Vijayaraghavan S (2003) Modulation of presynaptic store calcium induces release of glutamate and postsynaptic firing. Neuron 38: 929–939.
[40]  Bushong EA, Martone ME, Jones YZ, Ellisman MH (2002) Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22: 183–192.
[41]  Ventura R, Harris KM (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19: 6897–6906.
[42]  Bruno RM, Sakmann B (2006) Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312: 1622–1627.
[43]  Thomson AM, Bannister AP (2003) Interlaminar connections in the neocortex. Cereb Cortex 13: 5–14.
[44]  Douglas RJ, Martin KA (2004) Neuronal circuits of the neocortex. Annu Rev Neurosci 27: 419–451.
[45]  Shipp S (2007) Structure and function of the cerebral cortex. Curr Biol 17: R443–449.
[46]  Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, et al. (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8: 752–758.
[47]  Kirkwood A, Rozas C, Kirkwood J, Perez F, Bear MF (1999) Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. J Neurosci 19: 1599–1609.

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