[en] The efficient processing of visual information relies on a mature visual cortex, characterized by hierarchically organized areas and a broad diversity of inhibitory and excitatory neurons. A tightly regulated excitation-inhibition (E/I) balance is essential for the optimal processing of visual inputs. A known regulator of the cortical E/I balance is the endocannabinoid (ECB) system, which relies on the cannabinoid type-1 receptor (CB1R) to perform its functions. To better understand the embedding of the CB1R in the neuronal networks of the visual cortex in adolescence and adulthood, we characterized the distribution of the receptor protein and its mRNA (cnr1) across layers, areas, and interneuron subtypes. We describe a specific laminar distribution of CB1R in the mature visual cortex along the full extent of the rostrocaudal brain axis. Moreover, cnr1 is expressed in the three main nonoverlapping subtypes of interneurons and is predominantly enriched in the 5ht3ar subtypes. Comparison of adolescent and adult visual cortex revealed a higher number of cnr1+ reelin interneurons in layer 1 and a lower number of cnr1+ somatostatin interneurons in layer 4 of the primary visual cortex (V1) in adolescence compared with adulthood. Overall, our findings confirm a distinct distribution of the receptor in V1 compared with higher-order visual areas based on a lower CB1R expression in layer 4, a broad cnr1 expression across cortical interneurons in key locations of top-down modulation, and a still immature ECB system in adolescence, making it potentially vulnerable to exogenous cannabinoids during this life period.
Durieux, Lucas J A; KU Leuven, Department of Biology, Laboratory of Neuroplasticity and Neuroproteomics, Leuven, Belgium ; Leuven Brain Institute, Leuven, Belgium
Pereira, Maria João; KU Leuven, Department of Biology, Laboratory of Neuroplasticity and Neuroproteomics, Leuven, Belgium ; Leuven Brain Institute, Leuven, Belgium
VILLERS, Agnès ; Université de Mons - UMONS > Faculté de Médecine et de Pharmacie > Service de Neurosciences
Gilissen, Sara R J ✱; KU Leuven, Department of Biology, Laboratory of Neuroplasticity and Neuroproteomics, Leuven, Belgium ; Leuven Brain Institute, Leuven, Belgium
Arckens, Lutgarde ✱; KU Leuven, Department of Biology, Laboratory of Neuroplasticity and Neuroproteomics, Leuven, Belgium ; Leuven Brain Institute, Leuven, Belgium
✱ These authors have contributed equally to this work.
Language :
English
Title :
Age-Dependent Area-, Lamina- and Cell-Type-Specific Distribution of the Cannabinoid Type 1 Receptor in the Mouse Visual Cortex.
R550 - Institut des Sciences et Technologies de la Santé R100 - Institut des Biosciences
Funders :
Fundação para a Ciência e a Tecnologia Fonds Wetenschappelijk Onderzoek
Funding text :
This work was supported by the KU Leuven Research Council (C14/20/071), the Research Foundation Flanders (FWO), Belgium, via research project funding (G0C9922N) and a doctoral fellowship for L. J. A. Durieux (SB/1S62920N), and by FCT\u2014Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia via a doctoral fellowship for M.J. Pereira (2023.00418.BD). The funding sources were not involved in study design, collection, analyses, interpretation of the data, or active writing of this work. Figures were created with Adobe Illustrator 2024 (Adobe Systems, California, USA) and BioRender.com. We would like to thank Lieve Geenen and Evelien Herinckx for their technical expertise and support.
Beneyto, M., H. M. Morris, K. C. Rovensky, and D. A. Lewis. 2012. “Lamina- and Cell-Specific Alterations in Cortical Somatostatin Receptor 2 mRNA Expression in Schizophrenia.” Neuropharmacology 62, no. 3: 1598–1605. https://doi.org/10.1016/j.neuropharm.2010.12.029.
Bodor, Á.g. L., I. Katona, G. Nyíri, et al. 2005. “Endocannabinoid Signaling in Rat Somatosensory Cortex: Laminar Differences and Involvement of Specific Interneuron Types.” The Journal of Neuroscience 25, no. 29: 6845. https://doi.org/10.1523/JNEUROSCI.0442-05.2005.
Busquets-Garcia, A., J. F. Oliveira da Cruz, G. Terral, et al. 2018. “Hippocampal CB1 Receptors Control Incidental Associations.” Neuron 99, no. 6: 1247–1259.e7. https://doi.org/10.1016/J.NEURON.2018.08.014/ATTACHMENT/F8460464-8D4E-46FF-B5A3-521A00A5DB94/MMC2.PDF.
Butler, P. D., S. M. Silverstein, and S. C. Dakin. 2008. “Visual Perception and Its Impairment in Schizophrenia.” Biological Psychiatry 64, no. 1: 40. https://doi.org/10.1016/J.BIOPSYCH.2008.03.023.
Cadenhead, K. S., K. Dobkins, J. McGovern, and K. Shafer. 2013. “Schizophrenia Spectrum Participants Have Reduced Visual Contrast Sensitivity to Chromatic (Red/Green) and Luminance (Light/Dark) Stimuli: New Insights Into Information Processing, Visual Channel Function, and Antipsychotic Effects.” Frontiers in Psychology 4: 535. https://doi.org/10.3389/FPSYG.2013.00535.
Cauller, L. 1995. “Layer I of Primary Sensory Neocortex: Where Top-Down Converges Upon Bottom-Up.” Behavioural Brain Research 71, no. 1–2: 163–170. https://doi.org/10.1016/0166-4328(95)00032-1.
Chen, C. Y., A. C. Bonham, C. Dean, F. A. Hopp, C. J. Hillard, and J. L. Seagard. 2010. “Retrograde Release of Endocannabinoids Inhibits Presynaptic GABA Release to Second-Order Baroreceptive Neurons in NTS.” Autonomic Neuroscience: Basic and Clinical 158, no. 1–2: 44–50. https://doi.org/10.1016/j.autneu.2010.06.001.
Choi, H. M. T., C. R. Calvert, N. Husain, et al. 2016. “Mapping a Multiplexed Zoo of mRNA Expression.” Development (Cambridge) 143, no. 19: 3632–3637. https://doi.org/10.1242/DEV.140137/VIDEO-5.
Choi, H. M. T., M. Schwarzkopf, M. E. Fornace, et al. 2018. “Third-Generation in Situ Hybridization Chain Reaction: Multiplexed, Quantitative, Sensitive, Versatile, Robust.” Development (Cambridge) 145, no. 12: dev165753. https://doi.org/10.1242/DEV.165753.
Chou, S., T. Ranganath, K. N. Fish, D. A. Lewis, and R. A. Sweet. 2022. “Cell Type Specific Cannabinoid CB1 Receptor Distribution Across the Human and Non-Human Primate Cortex.” Scientific Reports 12, no. 1: 1–11. https://doi.org/10.1038/S41598-022-13724-X;SUBJMETA=1964,308,378,548,575,631,692;KWRD=NEUROTRANSMITTERS,TRANSLATIONAL+RESEARCH.
Davis, M. I., J. R. Crittenden, A. Y. Feng, et al. 2019. “The Cannabinoid-1 Receptor Is Abundantly Expressed in Striatal Striosomes and Striosome-Dendron Bouquets of the Substantia Nigra.” PLoS ONE 13, no. 2: e0191436. https://doi.org/10.1371/JOURNAL.PONE.0191436.
DeFelipe, J., and I. Fariñas. 1992. “The Pyramidal Neuron of the Cerebral Cortex: Morphological and Chemical Characteristics of the Synaptic Inputs.” Progress in Neurobiology 39, no. 6: 563–607. https://doi.org/10.1016/0301-0082(92)90015-7.
DeFelipe, J., and M. D. C. González-Albo. 1998. “Chandelier Cell Axons Are Immunoreactive for GAT-1 in the Human Neocortex.” Neuroreport 9, no. 3: 467–470. https://doi.org/10.1097/00001756-199802160-00020.
Deryckere, A., R. Styfhals, A. Murat Elagoz, G. E. Maes, and E. Seuntjens. 2021. “Identification of Neural Progenitor Cells and Their Progeny Reveals Long Distance Migration in the Developing Octopus Brain.” Elife 10: e69161. https://doi.org/10.7554/ELIFE.69161.
Doniger, G. M., J. J. Foxe, M. M. Murray, B. A. Higgins, and D. C. Javitt. 2002. “Impaired Visual Object Recognition and Dorsal/Ventral Stream Interaction in Schizophrenia.” Archives of General Psychiatry 59, no. 11: 1011–1020. https://doi.org/10.1001/archpsyc.59.11.1011.
D'Souza, R. D., Q. Wang, W. Ji, et al. 2022. “Hierarchical and Nonhierarchical Features of the Mouse Visual Cortical Network.” Nature Communications 13, no. 1: 503. https://doi.org/10.1038/S41467-022-28035-Y.
Durieux, L. J. A., S. R. J. Gilissen, and L. Arckens. 2021. “Endocannabinoids and Cortical Plasticity: CB1R as a Possible Regulator of the Excitation/Inhibition Balance in Health and Disease.” European Journal of Neuroscience 55: 971–988. https://doi.org/10.1111/ejn.15110.
Farishta, R. A., C. Robert, O. Turcot, et al. 2015. “Impact of CB1 Receptor Deletion on Visual Responses and Organization of Primary Visual Cortex in Adult Mice.” Investigative Ophthalmology and Visual Science 56, no. 13: 7697–7707. https://doi.org/10.1167/IOVS.15-17690.
Feldmeyer, D., G. Qi, V. Emmenegger, and J. F. Staiger. 2018. “Inhibitory Interneurons and Their Circuit Motifs in the Many Layers of the Barrel Cortex.” Neuroscience 368: 132–151. https://doi.org/10.1016/j.neuroscience.2017.05.027.
Fung, S. J., M. J. Webster, S. Sivagnanasundaram, C. Duncan, M. Elashoff, and C. S. Weickert. 2010. “Expression of Interneuron Markers in the Dorsolateral Prefrontal Cortex of the Developing Human and in Schizophrenia.” American Journal of Psychiatry 167, no. 12: 1479–1488. https://doi.org/10.1176/APPI.AJP.2010.09060784.
Garcia-Munoz, M., and G. W. Arbuthnott. 2015. “Basal Ganglia—Thalamus and the 'Crowning Enigma.” Frontiers in Neural Circuits 9, no. November: 1–10. https://doi.org/10.3389/FNCIR.2015.00071.
Gebreegziabhere, Y., K. Habatmu, A. Mihretu, M. Cella, and A. Alem. 2022. “Cognitive Impairment in People with Schizophrenia: an Umbrella Review.” European Archives of Psychiatry and Clinical Neuroscience 272, no. 7: 1139–1155. https://doi.org/10.1007/S00406-022-01416-6.
Goldbach, H. C., B. Akitake, C. E. Leedy, and M. H. Histed. 2021. “Performance in Even a Simple Perceptual Task Depends on Mouse Secondary Visual Areas.” Elife 10: 1–39. https://doi.org/10.7554/ELIFE.62156.
Gordon, J. A., M. P. Sttyker, N. G. Program, and W. M. Keck. 1996. “Experience-Dependent Plasticity of Binocular Responses in the Primary Visual Cortex of the Mouse.” Journal of Neuroscience 16, no. 10: 3274–3286. https://doi.org/10.1523/JNEUROSCI.16-10-03274.1996.
Haj-Dahmane, S., and R. Y.u Shen. 2011. “Modulation of the Serotonin System by Endocannabinoid Signaling.” Neuropharmacology 61, no. 3: 414. https://doi.org/10.1016/J.NEUROPHARM.2011.02.016.
Hao, Y., S. Hao, E. Andersen-Nissen, et al. 2021. “Integrated Analysis of Multimodal Single-Cell Data.” Cell 184, no. 13: 3573–3587.e29. https://doi.org/10.1016/J.CELL.2021.04.048/ASSET/13B1132E-1BA1-48C0-89F4-2EE6D8AB8FBA/MAIN.ASSETS/FIGS7.JPG.
Heinbockel, T., and A. Straiker. 2021. “Cannabinoids Regulate Sensory Processing in Early Olfactory and Visual Neural Circuits.” Frontiers in Neural Circuits 15: 662349. https://doi.org/10.3389/FNCIR.2021.662349/XML.
Hensch, T. K. 2005. “Critical Period Plasticity in Local Cortical Circuits.” Nature Reviews Neuroscience 6, no. 11: 877–888. https://doi.org/10.1038/nrn1787.
Hensch, T. K., and M. Fagiolini. 2005. “Excitatory-Inhibitory Balance and Critical Period Plasticity in Developing Visual Cortex.” Progress in Brain Research 147: (no. SPEC. ISS:.):115–124.
Hill, E. L., T. Gallopin, I. Férézou, et al. 2007. “Functional CB1 Receptors Are Broadly Expressed in Neocortical GABAergic and Glutamatergic Neurons.” Journal of Neurophysiology 97, no. 4: 2580–2589. https://doi.org/10.1152/JN.00603.2006.
Huang, S., and A. Kirkwood. 2020. “Endocannabinoid Signaling Contributes to Experience-Induced Increase of Synaptic Release Sites from Parvalbumin Interneurons in Mouse Visual Cortex.” Frontiers in Cellular Neuroscience 14: 571133. https://doi.org/10.3389/FNCEL.2020.571133.
Hubel, D. H., and T. N. Wiesel. 1962. “Receptive Fields, Binocular Interaction and Functional Architecture in the Cat's Visual Cortex.” The Journal of Physiology 160, no. 1: 106. https://doi.org/10.1113/JPHYSIOL.1962.SP006837.
Ibrahim, L. A., L. Mesik, X. Y., Ji, et al. 2016. “Cross-Modality Sharpening of Visual Cortical Processing Through Layer-1-Mediated Inhibition and Disinhibition.” Neuron 89, no. 5: 1031–1045. https://doi.org/10.1016/J.NEURON.2016.01.027.
Jiang, B., S. Huang, R. d. Pasquale, et al. 2010. “The Maturation of GABAergic Transmission in Visual Cortex Requires Endocannabinoid-Mediated LTD of Inhibitory Inputs During a Critical Period.” Neuron 66, no. 2: 248–259. https://doi.org/10.1016/j.neuron.2010.03.021.
Jiang, B., Z. J. Huang, B. Morales, and A. Kirkwood. 2005. “Maturation of GABAergic Transmission and the Timing of Plasticity in Visual Cortex.” Brain Research Reviews 50, no. 1: 126–133. https://doi.org/10.1016/j.brainresrev.2005.05.007.
Jiang, B., K. Sohya, A. Sarihi, Y. Yanagawa, and T. Tsumoto. 2010. “Laminar-Specific Maturation of GABAergic Transmission and Susceptibility to Visual Deprivation Are Related to Endocannabinoid Sensitivity in Mouse Visual Cortex.” Journal of Neuroscience 30, no. 42: 14261–14272. https://doi.org/10.1523/JNEUROSCI.2979-10.2010.
Jiang, B., M. Treviño, and A. Kirkwood. 2007. “Sequential Development of Long-Term Potentiation and Depression in Different Layers of the Mouse Visual Cortex.” The Journal of Neuroscience 27, no. 36: 9648. https://doi.org/10.1523/JNEUROSCI.2655-07.2007.
Jin, M., and L. L. Glickfeld. 2020. “Mouse Higher Visual Areas Provide both Distributed and Specialized Contributions to Visually Guided Behaviors.” Current Biology 30, no. 23: 4682–4692.e7. https://doi.org/10.1016/J.CUB.2020.09.015.
Khedr, E. M., Y. Elserogy, and G. K. Ahmed. 2025. “The Impact of Cannabis Use on Cortical Excitability and Inhibitory Mechanisms: A Case-Control Study.” Psychiatry Research 351: 116617. https://doi.org/10.1016/J.PSYCHRES.2025.116617.
Kim, D., V. Zemon, A. Saperstein, P. D. Butler, and D. C. Javitt. 2005. “Dysfunction of Early-Stage Visual Processing in Schizophrenia: Harmonic Analysis.” Schizophrenia Research 76, no. 1: 55–65. https://doi.org/10.1016/J.SCHRES.2004.10.011.
Kirkwood, A., H. Kyoung Lee, and M. F. Bear. 1995. “Co-Regulation of Long-Term Potentiation and Experience-Dependent Synaptic Plasticity in Visual Cortex by Age and Experience.” Nature 375, no. 6529: 328–331. https://doi.org/10.1038/375328A0.
Kiss, I., Á.g. Fábián, G. Benedek, and S. Kéri. 2010. “When Doors of Perception Open: Visual Contrast Sensitivity in Never-Medicated, First-Episode Schizophrenia.” Journal of Abnormal Psychology 119, no. 3: 586–593. https://doi.org/10.1037/A0019610.
Koukouli, F., M. Montmerle, A. Aguirre, et al. 2022. “Visual-Area-Specific Tonic Modulation of GABA Release by Endocannabinoids Sets the Activity and Coordination of Neocortical Principal Neurons.” Cell Reports 40, no. 8: 111202. https://doi.org/10.1016/j.celrep.2022.111202.
Kuehn, E., D. S. Clausen, R. W. Null, B. M. Metzger, A. D. Willis, and B. D. Özpolat. 2022. “Segment Number Threshold Determines Juvenile Onset of Germline Cluster Expansion in Platynereis Dumerilii.” Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 338, no. 4: 225–240. https://doi.org/10.1002/JEZ.B.23100.
Lee, S. H., J. Hjerling-Leffler, E. Zagha, G. Fishell, and B. Rudy. 2010. “The Largest Group of Superficial Neocortical GABAergic Interneurons Expresses Ionotropic Serotonin Receptors.” Journal of Neuroscience 30, no. 50: 16796–16808. https://doi.org/10.1523/JNEUROSCI.1869-10.2010.
Levelt, C. N., and M. Ḧubener. 2012. “Critical-Period Plasticity in the Visual Cortex.” Annual Review of Neuroscience 35: 309–330. https://doi.org/10.1146/ANNUREV-NEURO-061010-113813.
Lim, L., D.a Mi, A. Llorca, and O. Marín. 2018. “Development and Functional Diversification of Cortical Interneurons.” Neuron 100, no. 2: 294–313. https://doi.org/10.1016/j.neuron.2018.10.009.
Loı¨s, L.¨s, S. Miraucourt, J. Tsui, et al. 2016. “Endocannabinoid Signaling Enhances Visual Responses Through Modulation of Intracellular Chloride Levels in Retinal Ganglion Cells.” eLife 8, no. 5: e15932. https://doi.org/10.7554/eLife.15932.001.
Mariani, Y., A. Covelo, R. S. Rodrigues, et al. 2023. “Striatopallidal Cannabinoid Type-1 Receptors Mediate Amphetamine-Induced Sensitization.” Current Biology 33, no. 22: 5011–5022.e6. https://doi.org/10.1016/J.CUB.2023.09.075.
Marsicano, G., and B. Lutz. 1999. “Expression of the Cannabinoid Receptor CB1 in Distinct Neuronal Subpopulations in the Adult Mouse Forebrain.” European Journal of Neuroscience 11, no. 12: 4213–4225. https://doi.org/10.1046/J.1460-9568.1999.00847.X.
Martínez, A., S. A. Hillyard, E. C. Dias, et al. 2008. “Magnocellular Pathway Impairment in Schizophrenia: Evidence from Functional Magnetic Resonance Imaging.” Journal of Neuroscience 28, no. 30: 7492–7500. https://doi.org/10.1523/JNEUROSCI.1852-08.2008.
Mesik, L., J. J. Huang, L. I. Zhang, and H. W. Tao. 2019. “Sensory- And Motor-Related Responses of Layer 1 Neurons in the Mouse Visual Cortex.” Journal of Neuroscience 39, no. 50: 10060–10070. https://doi.org/10.1523/JNEUROSCI.1722-19.2019.
Micheva, K. D., M. Kiraly, M. M. Perez, and D. V. Madison. 2021. “Extensive Structural Remodeling of the Axonal Arbors of Parvalbumin Basket Cells During Development in Mouse Neocortex.” Journal of Neuroscience 41, no. 45: 9326–9339. https://doi.org/10.1523/JNEUROSCI.0871-21.2021.
Min, R., Y. Qin, S. Kerst, M. Hadi Saiepour, M. V. Lier, and C. N. Levelt. 2024. “Inhibitory Maturation and Ocular Dominance Plasticity in Mouse Visual Cortex Require Astrocyte CB1 Receptors.” Iscience 27, no. 12: 111410. https://doi.org/10.1016/J.ISCI.2024.111410.
Morales, M., S. D. Wang, O. Diaz-Ruiz, and D. H. J. Jho. 2004. “Cannabinoid CB1 Receptor and Serotonin 3 Receptor Subunit A (5-HT 3A) Are Co-Expressed in GABA Neurons in the Rat Telencephalon.” Journal of Comparative Neurology 468, no. 2: 205–216. https://doi.org/10.1002/CNE.10968.
Morris, H. M., T. Hashimoto, and D. A. Lewis. 2008. “Alterations in Somatostatin mRNA Expression in the Dorsolateral Prefrontal Cortex of Subjects with Schizophrenia or Schizoaffective Disorder.” Cerebral Cortex 18, no. 7: 1575–1587. https://doi.org/10.1093/CERCOR/BHM186.
Nabel, E. M., and H. Morishita. 2013. “Regulating Critical Period Plasticity: Insight from the Visual System to Fear Circuitry for Therapeutic Interventions.” Frontiers in Psychiatry 4, no. 146. https://doi.org/10.3389/FPSYT.2013.00146.
NCBI. “BLAST: Basic Local Alignment Search Tool.” Retrieved July 16, 2025. (https://blast.ncbi.nlm.nih.gov/Blast.cgi).
Nys, J., J. Aerts, E. Ytebrouck, et al. 2014. “The Cross-Modal Aspect of Mouse Visual Cortex Plasticity Induced by Monocular Enucleation Is Age Dependent.” Journal of Comparative Neurology 522, no. 4: 950–970. https://doi.org/10.1002/cne.23455.
Nys, J., K. Smolders, M.-E. Laramée, I. Hofman. T.-T. Hu, and L. Arckens. 2015. “Regional Specificity of GABAergic Regulation of Cross-Modal Plasticity in Mouse Visual Cortex After Unilateral Enucleation.” The Journal of Neuroscience 35, no. 32: 11174–11189. https://doi.org/10.1523/JNEUROSCI.3808-14.2015.
Oláh, S., M. Füle, G. Komlósi, et al. 2009. “Regulation of Cortical Microcircuits by Unitary GABA-Mediated Volume Transmission.” Nature 461, no. 7268: 1278–1281. https://doi.org/10.1038/NATURE08503.
Pardi, M. B., A. Schroeder, and J. J. Letzkus. 2023. “Probing Top-Down Information in Neocortical Layer 1.” Trends in Neurosciences 46, no. 1: 20–31. https://doi.org/10.1016/J.TINS.2022.11.001.
Paxinos, G., and K. Franklin. 2012. The Mouse Brain in Stereotaxic Coordinates, Fourth Edition. Academic Press.
Peters, K. Z., J. F. Cheer, and R. Tonini. 2021. “Modulating the Neuromodulators: Dopamine, Serotonin, and the Endocannabinoid System.” Trends in Neurosciences 44, no. 6: 464–477. https://doi.org/10.1016/J.TINS.2021.02.001.
Piomelli, D. 2003. “The Molecular Logic of Endocannabinoid Signalling.” Nature Reviews Neuroscience 4, no. 11: 873–884. https://doi.org/10.1038/NRN1247.
Revheim, N., P. D. Butler, I. Schechter, M. Jalbrzikowski, G. Silipo, and D. C. Javitt. 2006. “Reading Impairment and Visual Processing Deficits in Schizophrenia.” Schizophrenia Research 87, no. 1–3: 238–245. https://doi.org/10.1016/j.schres.2006.06.022.
Roth, M. M., J. C. Dahmen, D. R. Muir, F. Imhof, F. J. Martini, and S. B. Hofer. 2015. “Thalamic Nuclei Convey Diverse Contextual Information to Layer 1 of Visual Cortex.” Nature Neuroscience 19, no. 2: 299–307. https://doi.org/10.1038/nn.4197.
Schechter, I., P. D. Butler, V. M. Zemon, et al. 2005. “Impairments in Generation of Early-Stage Transient Visual Evoked Potentials to Magno- and Parvocellular-Selective Stimuli in Schizophrenia.” Clinical Neurophysiology 116, no. 9: 2204. https://doi.org/10.1016/J.CLINPH.2005.06.013.
Scheyltjens, I., and L. Arckens. 2016. “The Current Status of Somatostatin-Interneurons in Inhibitory Control of Brain Function and Plasticity.” Neural Plasticity 2016: 1–20. https://doi.org/10.1155/2016/8723623.
Schuman, B., S. Dellal, A. Prönneke, R. MacHold, and B. Rudy. 2021. “Neocortical Layer 1: an Elegant Solution to Top-Down and Bottom-Up Integration.” Annual Review of Neuroscience 44: 221. https://doi.org/10.1146/ANNUREV-NEURO-100520-012117.
Schuman, B., R. P. Machold, Y. Hashikawa, J. Fuzik, G. J. Fishell, and B. Rudy. 2019. “Four Unique Interneuron Populations Reside in Neocortical Layer 1.” Journal of Neuroscience 39, no. 1: 125–139. https://doi.org/10.1523/JNEUROSCI.1613-18.2018.
Shu, S., G. Ju, and L. Fan. 1988. “The Glucose Oxidase-DAB-Nickel Method in Peroxidase Histochemistry of the Nervous System.” Neuroscience Letters 85, no. 2: 169–171. https://doi.org/10.1016/0304-3940(88)90346-1.
Shum, C., L. Dutan, E. Annuario, et al. 2020. “Δ9-Tetrahydrocannabinol and 2-AG Decreases Neurite Outgrowth and Differentially Affects ERK1/2 and Akt Signaling in hiPSC-Derived Cortical Neurons.” Molecular and Cellular Neuroscience 103: 103463. https://doi.org/10.1016/J.MCN.2019.103463.
Silberberg, G., and H. Markram. 2007. “Disynaptic Inhibition Between Neocortical Pyramidal Cells Mediated by Martinotti Cells.” Neuron 53, no. 5: 735–746. https://doi.org/10.1016/j.neuron.2007.02.012.
Somogyi, P. 1977. “A Specific ‘Axo-Axonal’ Interneuron in the Visual Cortex of the Rat.” Brain Research 136, no. 2: 345–350. https://doi.org/10.1016/0006-8993(77)90808-3.
Sun, W., L. Wang, S. Li, X. Tie, and B. Jiang. 2015. “Layer-Specific Endocannabinoid-Mediated Long-Term Depression of GABAergic Neurotransmission onto Principal Neurons in Mouse Visual Cortex.” The European Journal of Neuroscience 42, no. 3: 1952–1965. https://doi.org/10.1111/ejn.12958.
Szabó, G. G., N. Lenkey, N. Holderith, T. Andrási, Z. Nusser, and N. Hájos. 2014. “Presynaptic Calcium Channel Inhibition Underlies CB1 Cannabinoid Receptor-Mediated Suppression of GABA Release.” Journal of Neuroscience 34, no. 23: 7958–7963. https://doi.org/10.1523/JNEUROSCI.0247-14.2014.
Tasic, B., V. Menon, T. N. Nguyen, et al. 2016. “Adult Mouse Cortical Cell Taxonomy Revealed by Single Cell Transcriptomics.” Nature Neuroscience 19, no. 2: 335–346. https://doi.org/10.1038/nn.4216.
Tasic, B., Z. Yao, L. T. Graybuck, et al. 2018. “Shared and Distinct Transcriptomic Cell Types Across Neocortical Areas.” Nature 563, no. 7729: 72–78. https://doi.org/10.1038/S41586-018-0654-5.
Tremblay, R., S. Lee, and B. Rudy. 2016. “GABAergic Interneurons in the Neocortex: from Cellular Properties to Circuits.” Neuron 91, no. 2: 260–292. https://doi.org/10.1016/J.NEURON.2016.06.033.
Urban-Ciecko, J., and A. L. Barth. 2016. “Somatostatin-Expressing Neurons in Cortical Networks.” Nature Reviews Neuroscience 17, no. 7: 401–409. https://doi.org/10.1038/nrn.2016.53.
Van der Gucht, E., P. R. Hof, L. V. Brussel, K. Burnat, and L. Arckens. 2007. “Neurofilament Protein and Neuronal Activity Markers Define Regional Architectonic Parcellation in the Mouse Visual Cortex.” Cerebral Cortex 17, no. 12: 2805–2819. https://doi.org/10.1093/cercor/bhm012.
Van houcke, J., V. Mariën, C. Zandecki, et al. 2021. “Aging Impairs the Essential Contributions of Non-Glial Progenitors to Neurorepair in the Dorsal Telencephalon of the Killifish Nothobranchius Furzeri.” Aging Cell 20, no. 9: e13464. https://doi.org/10.1111/ACEL.13464.
Wang, Q., and A. Burkhalter. 2007. “Area Map of Mouse Visual Cortex.” Journal of Comparative Neurology 502, no. 3: 339–357. https://doi.org/10.1002/cne.21286.
Yao, Z., C. T. J. van Velthoven, T. Nghi Nguyen, et al. 2021. “A Taxonomy of Transcriptomic Cell Types Across the Isocortex and Hippocampal Formation.” Cell 184, no. 12: 3222–3241.e26. https://doi.org/10.1016/j.cell.2021.04.021.
Yavorska, I., and M. Wehr. 2016. “Somatostatin-Expressing Inhibitory Interneurons in Cortical Circuits.” Frontiers in Neural Circuits 10, no. 16: 1–18. https://doi.org/10.3389/fncir.2016.00076.
Yazaki-Sugiyama, Y., S. Kang, H. Cteau, T. Fukai, and T. K. Hensch. 2009. “Bidirectional Plasticity in Fast-Spiking GABA Circuits by Visual Experience.” Nature 462: 218–221. https://doi.org/10.1038/nature08485.
Yoneda, T., K. Kameyama, K. Esumi, Y. Daimyo, M. Watanabe, and Y. Hata. 2013. “Developmental and Visual Input-Dependent Regulation of the CB1 Cannabinoid Receptor in the Mouse Visual Cortex.” PLoS ONE 8, no. 1: e53082. https://doi.org/10.1371/JOURNAL.PONE.0053082.
Zeisel, A., A. B. M͡oz-Manchado, S. Codeluppi, et al. 2015. “Cell Types in the Mouse Cortex and Hippocampus Revealed by Single-Cell RNA-Seq.” Science 347, no. 6226: 1138–1142. https://doi.org/10.1126/SCIENCE.AAA1934/SUPPL_FILE/ZEISEL-SM.PDF.
Zhu, Y., and J. J. Zhu. 2004. “Rapid Arrival and Integration of Ascending Sensory Information in Layer 1 Nonpyramidal Neurons and Tuft Dendrites of Layer 5 Pyramidal Neurons of the Neocortex.” Journal of Neuroscience 24, no. 6: 1272–1279. https://doi.org/10.1523/JNEUROSCI.4805-03.2004.
