A subpopulation of astrocytes on the brain's surface, known as subpial astrocytes, constitutes the "glia limitans superficialis" (GLS), which is an interface between the brain parenchyma and the cerebrospinal fluid (CSF) in the subpial space. Changes in connexin-43 (Cx43) and aquaporin-4 (AQP4) proteins in subpial astrocytes were examined in the medial prefrontal cortex at postoperative day 1, 3, 7, 14, and 21 after sham operation and sciatic nerve compression (SNC). In addition, we tested the altered uptake of TRITC-conjugated 3 kDa dextran by reactive subpial astrocytes. Cellular immunofluorescence (IF) detection and image analysis were used to examine changes in Cx43 and AQP4 protein levels, as well as TRITC-conjugated 3 kDa dextran, in subpial astrocytes. The intensity of Cx43-IF was significantly increased, but AQP4-IF decreased in subpial astrocytes of sham- and SNC-operated rats during all survival periods compared to naïve controls. Similarly, the uptake of 3 kDa dextran in the GLS was reduced following both sham and SNC operations. The results suggest that both sciatic nerve injury and peripheral tissue injury alone can induce changes in subpial astrocytes related to the spread of their reactivity across the cortical surface mediated by increased amounts of gap junctions. At the same time, water transport and solute uptake were impaired in subpial astrocytes.

Cellular and Molecular Neurobiology Research Group Department of Anatomy Faculty of Medicine Masaryk University CZ 62500 Brno Czech Republic

Zobrazit více v PubMed

Giovannoni F., Quintana F.J. The Role of Astrocytes in CNS Inflammation. Trends Immunol. 2020;41:805–819. doi: 10.1016/j.it.2020.07.007. PubMed DOI PMC

Anderson M.A., Ao Y., Sofroniew M.V. Heterogeneity of Reactive Astrocytes. Neurosci. Lett. 2014;565:23–29. doi: 10.1016/j.neulet.2013.12.030. PubMed DOI PMC

Miller S.J. Astrocyte Heterogeneity in the Adult Central Nervous System. Front. Cell. Neurosci. 2018;12:401. doi: 10.3389/fncel.2018.00401. PubMed DOI PMC

Rakic P. Elusive Radial Glial Cells: Historical and Evolutionary Perspective. Glia. 2003;43:19–32. doi: 10.1002/glia.10244. PubMed DOI

Engelhardt B., Coisne C. Fluids and Barriers of the CNS Establish Immune Privilege by Confining Immune Surveillance to a Two-Walled Castle Moat Surrounding the CNS Castle. Fluids Barriers CNS. 2011;8:4. doi: 10.1186/2045-8118-8-4. PubMed DOI PMC

Liu X., Zhang Z., Guo W., Burnstock G., He C., Xiang Z. The Superficial Glia Limitans of Mouse and Monkey Brain and Spinal Cord: Glia Limitans of Brain and Spinal Cord. Anat. Rec. 2013;296:995–1007. doi: 10.1002/ar.22717. PubMed DOI

Verkhratsky A., Butt A.M. Chapter 3—Astroglial Physiology. In: Verkhratsky A., Butt A.M., editors. Neuroglia. Academic Press, Ltd.; London, UK: 2023. pp. 89–197.

Weller R.O., Sharp M.M., Christodoulides M., Carare R.O., Møllgård K. The Meninges as Barriers and Facilitators for the Movement of Fluid, Cells and Pathogens Related to the Rodent and Human CNS. Acta Neuropathol. 2018;135:363–385. doi: 10.1007/s00401-018-1809-z. PubMed DOI

Abbott N.J., Pizzo M.E., Preston J.E., Janigro D., Thorne R.G. The Role of Brain Barriers in Fluid Movement in the CNS: Is There a ‘Glymphatic’ System? Acta Neuropathol. 2018;135:387–407. doi: 10.1007/s00401-018-1812-4. PubMed DOI

Eto K., Kim S.K., Takeda I., Nabekura J. The Roles of Cortical Astrocytes in Chronic Pain and Other Brain Pathologies. Neurosci. Res. 2018;126:3–8. doi: 10.1016/j.neures.2017.08.009. PubMed DOI

Boulay A.-C., Gilbert A., Moreira V.O., Blugeon C., Perrin S., Pouch J., Le Crom S., Ducos B., Cohen-Salmon M. Connexin 43 Controls the Astrocyte Immunoregulatory Phenotype. Brain Sci. 2018;8:50. doi: 10.3390/brainsci8040050. PubMed DOI PMC

Nagy J.I., Rash J.E. Cx36, Cx43 and Cx45 in Mouse and Rat Cerebellar Cortex: Species-Specific Expression, Compensation in Cx36 Null Mice and Co-Localization in Neurons vs. Glia. Eur. J. Neurosci. 2017;46:1790–1804. doi: 10.1111/ejn.13614. PubMed DOI

Kielian T. Glial Connexins and Gap Junctions in CNS Inflammation and Disease. J. Neurochem. 2008;106:1000–1016. doi: 10.1111/j.1471-4159.2008.05405.x. PubMed DOI PMC

Iliff J.J., Wang M., Liao Y., Plogg B.A., Peng W., Gundersen G.A., Benveniste H., Vates G.E., Deane R., Goldman S.A., et al. A Paravascular Pathway Facilitates CSF Flow through the Brain Parenchyma and the Clearance of Interstitial Solutes, Including Amyloid β. Sci. Transl. Med. 2012;4:147ra111. doi: 10.1126/scitranslmed.3003748. PubMed DOI PMC

Mestre H., Hablitz L.M., Xavier A.L., Feng W., Zou W., Pu T., Monai H., Murlidharan G., Castellanos Rivera R.M., Simon M.J., et al. Aquaporin-4-Dependent Glymphatic Solute Transport in the Rodent Brain. eLife. 2018;7:e40070. doi: 10.7554/eLife.40070. PubMed DOI PMC

Zhou Z., Zhan J., Cai Q., Xu F., Chai R., Lam K., Luan Z., Zhou G., Tsang S., Kipp M., et al. The Water Transport System in Astrocytes–Aquaporins. Cells. 2022;11:2564. doi: 10.3390/cells11162564. PubMed DOI PMC

Patabendige A., Singh A., Jenkins S., Sen J., Chen R. Astrocyte Activation in Neurovascular Damage and Repair Following Ischaemic Stroke. Int. J. Mol. Sci. 2021;22:4280. doi: 10.3390/ijms22084280. PubMed DOI PMC

Cohen-Salmon M., Slaoui L., Mazaré N., Gilbert A., Oudart M., Alvear-Perez R., Elorza-Vidal X., Chever O., Boulay A.-C. Astrocytes in the Regulation of Cerebrovascular Functions. Glia. 2021;69:817–841. doi: 10.1002/glia.23924. PubMed DOI

Beggs S., Liu X.J., Kwan C., Salter M.W. Peripheral Nerve Injury and TRPV1-Expressing Primary Afferent C-Fibers Cause Opening of the Blood-Brain Barrier. Mol. Pain. 2010;6:74. doi: 10.1186/1744-8069-6-74. PubMed DOI PMC

Li Q.-Y., Chen S.-X., Liu J.-Y., Yao P.-W., Duan Y.-W., Li Y.-Y., Zang Y. Neuroinflammation in the Anterior Cingulate Cortex: The Potential Supraspinal Mechanism Underlying the Mirror-Image Pain Following Motor Fiber Injury. J. Neuroinflamm. 2022;19:162. doi: 10.1186/s12974-022-02525-8. PubMed DOI PMC

Austin P.J., Fiore N.T. Supraspinal Neuroimmune Crosstalk in Chronic Pain States. Curr. Opin. Physiol. 2019;11:7–15. doi: 10.1016/j.cophys.2019.03.008. DOI

Joukal M., Klusáková I., Solár P., Kuklová A., Dubový P. Cellular Reactions of the Choroid Plexus Induced by Peripheral Nerve Injury. Neurosci. Lett. 2016;628:73–77. doi: 10.1016/j.neulet.2016.06.019. PubMed DOI

Dellarole A., Morton P., Brambilla R., Walters W., Summers S., Bernardes D., Grilli M., Bethea J.R. Neuropathic Pain-Induced Depressive-like Behavior and Hippocampal Neurogenesis and Plasticity Are Dependent on TNFR1 Signaling. Brain. Behav. Immun. 2014;41:65–81. doi: 10.1016/j.bbi.2014.04.003. PubMed DOI PMC

Zhuo M. Neural Mechanisms Underlying Anxiety–Chronic Pain Interactions. Trends Neurosci. 2016;39:136–145. doi: 10.1016/j.tins.2016.01.006. PubMed DOI

Sang K., Bao C., Xin Y., Hu S., Gao X., Wang Y., Bodner M., Zhou Y.-D., Dong X.-W. Plastic Change of Prefrontal Cortex Mediates Anxiety-like Behaviors Associated with Chronic Pain in Neuropathic Rats. Mol. Pain. 2018;14:1744806918783931. doi: 10.1177/1744806918783931. PubMed DOI PMC

Bretová K., Svobodová V., Dubový P. Astrocyte Reactivity in the Glia Limitans Superficialis of the Rat Medial Prefrontal Cortex Following Sciatic Nerve Injury. Histochem. Cell Biol. 2023;159:185–198. doi: 10.1007/s00418-022-02161-6. PubMed DOI

Wagner H.-J., Barthel J., Pilgrim C. Permeability of the External Glial Limiting Membrane of Rat Parietal Cortex. Anat. Embryol. 1983;166:427–437. doi: 10.1007/BF00305928. PubMed DOI

Rite I., Machado A., Cano J., Venero J.L. Intracerebral VEGF Injection Highly Upregulates AQP4 mRNA and Protein in the Perivascular Space and Glia Limitans Extema. Neurochem. Int. 2008;52:897–903. doi: 10.1016/j.neuint.2007.10.004. PubMed DOI

Hoddevik E.H., Khan F.H., Rahmani S., Ottersen O.P., Boldt H.B., Amiry-Moghaddam M. Factors Determining the Density of AQP4 Water Channel Molecules at the Brain–Blood Interface. Brain Struct. Funct. 2017;222:1753–1766. doi: 10.1007/s00429-016-1305-y. PubMed DOI PMC

Markou A., Kitchen P., Aldabbagh A., Repici M., Salman M.M., Bill R.M., Balklava Z. Mechanisms of Aquaporin-4 Vesicular Trafficking in Mammalian Cells. J. Neurochem. 2024;168:100–114. doi: 10.1111/jnc.16029. PubMed DOI PMC

Mastorakos P., McGavern D. The Anatomy and Immunology of Vasculature in the Central Nervous System. Sci. Immunol. 2019;4:eaav0492. doi: 10.1126/sciimmunol.aav0492. PubMed DOI PMC

Pannasch U., Rouach N. Emerging Role for Astroglial Networks in Information Processing: From Synapse to Behavior. Trends Neurosci. 2013;36:405–417. doi: 10.1016/j.tins.2013.04.004. PubMed DOI

Dong A., Liu S., Li Y. Gap Junctions in the Nervous System: Probing Functional Connections Using New Imaging Approaches. Front. Cell. Neurosci. 2018;12:320. doi: 10.3389/fncel.2018.00320. PubMed DOI PMC

Weber P.A., Chang H.-C., Spaeth K.E., Nitsche J.M., Nicholson B.J. The Permeability of Gap Junction Channels to Probes of Different Size Is Dependent on Connexin Composition and Permeant-Pore Affinities. Biophys. J. 2004;87:958–973. doi: 10.1529/biophysj.103.036350. PubMed DOI PMC

Brightman M.W., Reese T.S. Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol. 1969;40:648–677. doi: 10.1083/jcb.40.3.648. PubMed DOI PMC

Metz A.E., Yau H.-J., Centeno M.V., Apkarian A.V., Martina M. Morphological and Functional Reorganization of Rat Medial Prefrontal Cortex in Neuropathic Pain. Proc. Natl. Acad. Sci. USA. 2009;106:2423–2428. doi: 10.1073/pnas.0809897106. PubMed DOI PMC

Fiore N.T., Austin P.J. Peripheral Nerve Injury Triggers Neuroinflammation in the Medial Prefrontal Cortex and Ventral Hippocampus in a Subgroup of Rats with Coincident Affective Behavioural Changes. Neuroscience. 2019;416:147–167. doi: 10.1016/j.neuroscience.2019.08.005. PubMed DOI

Kummer K.K., Mitrić M., Kalpachidou T., Kress M. The Medial Prefrontal Cortex as a Central Hub for Mental Comorbidities Associated with Chronic Pain. Int. J. Mol. Sci. 2020;21:3440. doi: 10.3390/ijms21103440. PubMed DOI PMC

Chen G., Park C.-K., Xie R.-G., Berta T., Nedergaard M., Ji R.-R. Connexin-43 Induces Chemokine Release from Spinal Cord Astrocytes to Maintain Late-Phase Neuropathic Pain in Mice. Brain. 2014;137:2193–2209. doi: 10.1093/brain/awu140. PubMed DOI PMC

Chen F.-L., Dong Y.-L., Zhang Z.-J., Cao D.-L., Xu J., Hui J., Zhu L., Gao Y.-J. Activation of Astrocytes in the Anterior Cingulate Cortex Contributes to the Affective Component of Pain in an Inflammatory Pain Model. Brain Res. Bull. 2012;87:60–66. doi: 10.1016/j.brainresbull.2011.09.022. PubMed DOI

Doyen P.J., Vergouts M., Pochet A., Desmet N., van Neerven S., Brook G., Hermans E. Inflammation-Associated Regulation of RGS in Astrocytes and Putative Implication in Neuropathic Pain. J. Neuroinflamm. 2017;14:209. doi: 10.1186/s12974-017-0971-x. PubMed DOI PMC

Morioka N., Nakamura Y., Zhang F.F., Hisaoka-Nakashima K., Nakata Y. Role of Connexins in Chronic Pain and Their Potential as Therapeutic Targets for Next-Generation Analgesics. Biol. Pharm. Bull. 2019;42:857–866. doi: 10.1248/bpb.b19-00195. PubMed DOI

Xing L., Yang T., Cui S., Chen G. Connexin Hemichannels in Astrocytes: Role in CNS Disorders. Front. Mol. Neurosci. 2019;12:23. doi: 10.3389/fnmol.2019.00023. PubMed DOI PMC

Donnelly C.R., Andriessen A.S., Chen G., Wang K., Jiang C., Maixner W., Ji R.-R. Central Nervous System Targets: Glial Cell Mechanisms in Chronic Pain. Neurotherapeutics. 2020;17:846–860. doi: 10.1007/s13311-020-00905-7. PubMed DOI PMC

Ye Z.-C., Wyeth M.S., Baltan-Tekkok S., Ransom B.R. Functional Hemichannels in Astrocytes: A Novel Mechanism of Glutamate Release. J. Neurosci. 2003;23:3588–3596. doi: 10.1523/JNEUROSCI.23-09-03588.2003. PubMed DOI PMC

Bennett M.V.L., Contreras J.E., Bukauskas F.F., Sáez J.C. New Roles for Astrocytes: Gap Junction Hemichannels Have Something to Communicate. Trends Neurosci. 2003;26:610–617. doi: 10.1016/j.tins.2003.09.008. PubMed DOI PMC

Giaume C., Leybaert L., Naus C.C., Saez J.C. Connexin and Pannexin Hernichannels in Brain Glial Cells: Properties, Pharmacology, and Roles. Front. Pharmacol. 2013;4:88. doi: 10.3389/fphar.2013.00088. PubMed DOI PMC

Jiang H., Zhang Y., Wang Z.-Z., Chen N.-H. Connexin 43: An Interface Connecting Neuroinflammation to Depression. Molecules. 2023;28:1820. doi: 10.3390/molecules28041820. PubMed DOI PMC

Dubový P. Wallerian Degeneration and Peripheral Nerve Conditions for Both Axonal Regeneration and Neuropathic Pain Induction. Ann. Anat.-Anat. Anz. 2011;193:267–275. doi: 10.1016/j.aanat.2011.02.011. PubMed DOI

Gaudet A.D., Popovich P.G., Ramer M.S. Wallerian Degeneration: Gaining Perspective on Inflammatory Events after Peripheral Nerve Injury. J. Neuroinflamm. 2011;8:110. doi: 10.1186/1742-2094-8-110. PubMed DOI PMC

Verkman A.S. Aquaporin Water Channels and Endothelial Cell Function. J. Anat. 2002;200:617–627. doi: 10.1046/j.1469-7580.2002.00058.x. PubMed DOI PMC

Manley G.T., Binder D.K., Papadopoulos M.C., Verkman A.S. New Insights into Water Transport and Edema in the Central Nervous System from Phenotype Analysis of Aquaporin-4 Null Mice. Neuroscience. 2004;129:983–991. doi: 10.1016/j.neuroscience.2004.06.088. PubMed DOI

Vindedal G.F., Thoren A.E., Jensen V., Klungland A., Zhang Y., Holtzman M.J., Ottersen O.P., Nagelhus E.A. Removal of Aquaporin-4 from Glial and Ependymal Membranes Causes Brain Water Accumulation. Mol. Cell. Neurosci. 2016;77:47–52. doi: 10.1016/j.mcn.2016.10.004. PubMed DOI PMC

Nesic O., Lee J., Ye Z., Unabia G.C., Rafati D., Hulsebosch C.E., Perez-Polo J.R. Acute and Chronic Changes in Aquaporin 4 Expression after Spinal Cord Injury. Neuroscience. 2006;143:779–792. doi: 10.1016/j.neuroscience.2006.08.079. PubMed DOI PMC

Chen G.Y., Nuñez G. Sterile Inflammation: Sensing and Reacting to Damage. Nat. Rev. Immunol. 2010;10:826–837. doi: 10.1038/nri2873. PubMed DOI PMC

Chiang C.-Y., Sessle B.J., Dostrovsky J.O. Role of Astrocytes in Pain. Neurochem. Res. 2012;37:2419–2431. doi: 10.1007/s11064-012-0801-6. PubMed DOI

Bojarskaite L., Nafari S., Ravnanger A.K., Frey M.M., Skauli N., Åbjørsbråten K.S., Roth L.C., Amiry-Moghaddam M., Nagelhus E.A., Ottersen O.P., et al. Role of Aquaporin-4 Polarization in Extracellular Solute Clearance. Fluids Barriers CNS. 2024;21:28. doi: 10.1186/s12987-024-00527-7. PubMed DOI PMC

In ’T Veen J.P.M., Van Den Berg M.P., Romeijn S.G., Verhoef J.C., Merkus F.W.H.M. Uptake of Fluorescein Isothiocyanate-Labelled Dextran into the CSF after Intranasal and Intravenous Administration to Rats. Eur. J. Pharma. Biopharma. 2005;61:27–31. doi: 10.1016/j.ejpb.2005.02.015. PubMed DOI

Matter K., Balda M.S. Functional Analysis of Tight Junctions. Methods. 2003;30:228–234. doi: 10.1016/S1046-2023(03)00029-X. PubMed DOI

Lippoldt A., Liebner S., Andbjer B., Kalbacher H., Wolburg H., Haller H., Fuxe K. Organization of Choroid Plexus Epithelial and Endothelial Cell Tight Junctions and Regulation of Claudin-1, -2 and -5 Expression by Protein Kinase C. NeuroReport. 2000;11:1427. doi: 10.1097/00001756-200005150-00015. PubMed DOI

Kratzer I., Ek J., Stolp H. The Molecular Anatomy and Functions of the Choroid Plexus in Healthy and Diseased Brain. Biochim. Biophys. Acta Biomembr. 2020;1862:183430. doi: 10.1016/j.bbamem.2020.183430. PubMed DOI

Katoozi S., Skauli N., Zahl S., Deshpande T., Ezan P., Palazzo C., Steinhäuser C., Frigeri A., Cohen-Salmon M., Ottersen O.P., et al. Uncoupling of the Astrocyte Syncytium Differentially Affects AQP4 Isoforms. Cells. 2020;9:382. doi: 10.3390/cells9020382. PubMed DOI PMC

Rao S.B., Skauli N., Jovanovic N., Katoozi S., Frigeri A., Froehner S.C., Adams M.E., Ottersen O.P., Amiry-Moghaddam M. Orchestrating Aquaporin-4 and Connexin-43 Expression in Brain: Differential Roles of A1- and Β1-Syntrophin. Biochim. Biophys. Acta Biomembr. 2021;1863:183616. doi: 10.1016/j.bbamem.2021.183616. PubMed DOI

Kim S.K., Hayashi H., Ishikawa T., Shibata K., Shigetomi E., Shinozaki Y., Inada H., Roh S.E., Kim S.J., Lee G., et al. Cortical Astrocytes Rewire Somatosensory Cortical Circuits for Peripheral Neuropathic Pain. J. Clin. Investig. 2016;126:1983. doi: 10.1172/JCI82859. PubMed DOI PMC

Kurabe M., Sasaki M., Furutani K., Furue H., Kamiya Y., Baba H. Structural and Functional Properties of Spinal Dorsal Horn Neurons after Peripheral Nerve Injury Change Overtime via Astrocyte Activation. iScience. 2022;25:105555. doi: 10.1016/j.isci.2022.105555. PubMed DOI PMC

Lawrence J.M., Schardien K., Wigdahl B., Nonnemacher M.R. Roles of Neuropathology-Associated Reactive Astrocytes: A Systematic Review. Acta Neuropathol. Commun. 2023;11:42. doi: 10.1186/s40478-023-01526-9. PubMed DOI PMC

Jean-Toussaint R., Tian Y., Chaudhuri A.D., Haughey N.J., Sacan A., Ajit S.K. Proteome Characterization of Small Extracellular Vesicles from Spared Nerve Injury Model of Neuropathic Pain. J. Proteom. 2020;211:103540. doi: 10.1016/j.jprot.2019.103540. PubMed DOI PMC

Luo X., Jean-Toussaint R., Tian Y., Balashov S.V., Sacan A., Ajit S.K. Small Extracellular Vesicles From Spared Nerve Injury Model and Sham Control Mice Differentially Regulate Gene Expression in Primary Microglia. J. Pain. 2023;24:1570–1581. doi: 10.1016/j.jpain.2023.03.015. PubMed DOI PMC

Tang Y., Wu J., Liu C., Gan L., Chen H., Sun Y.-L., Liu J., Tao Y.-X., Zhu T., Chen C. Schwann Cell-Derived Extracellular Vesicles Promote Memory Impairment Associated with Chronic Neuropathic Pain. J. Neuroinflamm. 2024;21:99. doi: 10.1186/s12974-024-03081-z. PubMed DOI PMC

Wang L., Lu X., Szalad A., Liu X.S., Zhang Y., Wang X., Golembieski W.A., Powell B., Mccann M., Lu M., et al. Schwann Cell-Derived Exosomes Ameliorate Peripheral Neuropathy Induced by Ablation of Dicer in Schwann Cells. Front. Cell. Neurosci. 2024;18:1462228. doi: 10.3389/fncel.2024.1462228. PubMed DOI PMC

Zhang C., Gao R., Zhou R., Chen H., Liu C., Zhu T., Chen C. The Emerging Power and Promise of Non-Coding RNAs in Chronic Pain. Front. Mol. Neurosci. 2022;15:1037929. doi: 10.3389/fnmol.2022.1037929. PubMed DOI PMC

He X., Yang H., Zheng Y., Zhao X., Wang T. The Role of Non-Coding RNAs in Neuropathic Pain. Pflugers Arch.-Eur. J. Physiol. 2024;476:1625–1643. doi: 10.1007/s00424-024-02989-y. PubMed DOI

Jullienne A., Fukuda A.M., Ichkova A., Nishiyama N., Aussudre J., Obenaus A., Badaut J. Modulating the Water Channel AQP4 Alters miRNA Expression, Astrocyte Connectivity and Water Diffusion in the Rodent Brain. Sci. Rep. 2018;8:4186. doi: 10.1038/s41598-018-22268-y. PubMed DOI PMC

Xian S., Ding R., Li M., Chen F. LncRNA NEAT1/miR-128-3p/AQP4 Axis Regulating Spinal Cord Injury-Induced Neuropathic Pain Progression. J. Neuroimmunol. 2021;351:577457. doi: 10.1016/j.jneuroim.2020.577457. PubMed DOI

Neumann E., Hermanns H., Barthel F., Werdehausen R., Brandenburger T. Expression Changes of MicroRNA-1 and Its Targets Connexin 43 and Brain-Derived Neurotrophic Factor in the Peripheral Nervous System of Chronic Neuropathic Rats. Mol. Pain. 2015;11:39. doi: 10.1186/s12990-015-0045-y. PubMed DOI PMC

Yi Y., Zhang S., Dai J., Zheng H., Peng X., Cheng L., Chen H., Hu Y. MiR-23b-3p Improves Brain Damage after Status Epilepticus by Reducing the Formation of Pathological High-Frequency Oscillations via Inhibition of Cx43 in Rat Hippocampus. ACS Chem. Neurosci. 2024;15:2633–2642. doi: 10.1021/acschemneuro.4c00112. PubMed DOI

EL Andaloussi S., Mäger I., Breakefield X.O., Wood M.J.A. Extracellular Vesicles: Biology and Emerging Therapeutic Opportunities. Nat. Rev. Drug Discov. 2013;12:347–357. doi: 10.1038/nrd3978. PubMed DOI

Zamboni L., Demartin C. Buffered Picric Acid-Formaldehyde—A New Rapid Fixative for Electron Microscopy. J. Cell Biol. 1967;35:A148

Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates. J. Anat. 1997;191:315–317. doi: 10.1046/j.1469-7580.1997.191203153.x. DOI

Hylden J.L.K., Wilcox G.L. Intrathecal Morphine in Mice: A New Technique. Eur. J. Pharmacol. 1980;67:313–316. doi: 10.1016/0014-2999(80)90515-4. PubMed DOI

Dubový P., Svízenská I., Klusáková I. Computer-Assisted Quantitative Analysis of Immunofluorescence Staining of the Extracellular Matrix in Rat Dorsal and Ventral Spinal Roots. Acta Histochem. 2002;104:371–374. doi: 10.1078/0065-1281-00664. PubMed DOI