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Deletion of p75NTR enhances the cholinergic innervation pattern of the visual cortex

Published online by Cambridge University Press:  17 October 2016

VIOLA VON BOHLEN UND HALBACH  and
OLIVER VON BOHLEN UND HALBACH
VIOLA VON BOHLEN UND HALBACH
Affiliation:
Institute of Anatomy and Cell Biology, Universitätsmedizin Greifswald, 17487 Greifswald, Germany
OLIVER VON BOHLEN UND HALBACH*
Affiliation:
Institute of Anatomy and Cell Biology, Universitätsmedizin Greifswald, 17487 Greifswald, Germany
*
*Address correspondence to: Oliver von Bohlen und Halbach, Institute of Anatomy and Cell Biology, Universitätsmedizin Greifswald, Friedrich Loeffler Strasse 23c, 17487 Greifswald, Germany. E-mail: [email protected]
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Abstract

The cholinergic system is involved in cortical plasticity, attention, and learning. Within the visual cortex the cholinergic system seems to play a role in visual perception. The cholinergic neurons which project into the visual cortex are located in the basal forebrain. It has been shown that mice deficient for the low-affinity neurotrophin receptor p75NTR display increased numbers of cholinergic neurons in the basal forebrain and a denser cholinergic innervation of the hippocampus. This prompted us to analyze whether the cholinergic system is altered in adult p75NTR deficient mice. By analyzing the densities of cholinergic fibers within layer IV as well as within layer V of the visual cortex, we found that adult p75NTR deficient mice display increased cholinergic fiber densities. However, this increase was not accompanied by an increase in the density of local cholinergic neurons within the visual cortex. This indicates that the enhanced cholinergic innervation of the visual cortex is due to alteration of the cholinergic neurons located in the basal forebrain, projecting to the visual cortex. The increased cholinergic innervation of the visual cortex makes the p75NTR deficient mice an attractive model to study the necessity of the cholinergic system for the visual cortex.

Keywords

Acetylcholinep75NTRCholinergic innervationImmunohistochemistryCortex
Type
Research Article
Information
Visual Neuroscience , Volume 33 , 2016 , E012
Copyright
Copyright © Cambridge University Press 2016 

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References

Baryshnikova, L.M., von Bohlen und Halbach, O., Kaplan, S. & von Bartheld, C.S. (2006). Two distinct events, section compression and loss of particles (“lost caps”), contribute to z-axis distortion and bias in optical disector counting. Microscopy Research and Technique 69, 738–756.CrossRefGoogle ScholarPubMed
Bogenmann, E., Thomas, P.S., Li, Q., Kim, J., Yang, L.T., Pierchala, B. & Kaartinen, V. (2011). Generation of mice with a conditional allele for the p75(NTR) neurotrophin receptor gene. Genesis 49, 862–869.CrossRefGoogle ScholarPubMed
Boissiere, F., Faucheux, B., Agid, Y. & Hirsch, E.C. (1997). Expression of catalytic trkB gene in the striatum and the basal forebrain of patients with Alzheimer’s disease: An in situ hybridization study. Neuroscience Letters 221, 141–144.Google Scholar
Brocher, S., Artola, A. & Singer, W. (1992). Agonists of cholinergic and noradrenergic receptors facilitate synergistically the induction of long-term potentiation in slices of rat visual cortex. Brain Research 573, 27–36.Google Scholar
Bruel-Jungerman, E., Lucassen, P.J. & Francis, F. (2011). Cholinergic influences on cortical development and adult neurogenesis. Behavioural Brain Research 221, 379–388.Google Scholar
Chourbaji, S., Hellweg, R., Brandis, D., Zorner, B., Zacher, C., Lang, U.E., Henn, F.A., Hortnagl, H. & Gass, P. (2004). Mice with reduced brain-derived neurotrophic factor expression show decreased choline acetyltransferase activity, but regular brain monoamine levels and unaltered emotional behavior. Molecular Brain Research 121, 28–36.CrossRefGoogle ScholarPubMed
Consonni, S., Leone, S., Becchetti, A. & Amadeo, A. (2009). Developmental and neurochemical features of cholinergic neurons in the murine cerebral cortex. BMC Neuroscience 10, 18.CrossRefGoogle ScholarPubMed
Dokter, M., Busch, R., Poser, R., Vogt, M.A., von Bohlen und Halbach, V., Gass, P., Unsicker, K. & von Bohlen und Halbach, O. (2015). Implications of p75NTR for dentate gyrus morphology and hippocampus-related behavior revisited. Brain Structure & Function 220, 1449–1462.Google Scholar
Fagan, A.M., Garber, M., Barbacid, M., Silos-Santiago, I. & Holtzman, D.M. (1997). A role for TrkA during maturation of striatal and basal forebrain cholinergic neurons in vivo . The Journal of Neuroscience 17, 7644–7654.CrossRefGoogle ScholarPubMed
Franklin, K.B.J. & Paxinos, G. (2007). The Mouse Brain in Stereotaxic Coordinates. New York: Academic Press.Google Scholar
Greferath, U., Bennie, A., Kourakis, A., Bartlett, P.F., Murphy, M. & Barrett, G.L. (2000). Enlarged cholinergic forebrain neurons and improved spatial learning in p75 knockout mice. European Journal of Neuroscience 12, 885–893.CrossRefGoogle ScholarPubMed
Gu, Q. (2003). Contribution of acetylcholine to visual cortex plasticity. Neurobiology of Learning and Memory 80, 291–301.Google Scholar
Heckers, S., Ohtake, T., Wiley, R.G., Lappi, D.A., Geula, C. & Mesulam, M.M. (1994). Complete and selective cholinergic denervation of rat neocortex and hippocampus but not amygdala by an immunotoxin against the p75 NGF receptor. The Journal of Neuroscience 14, 1271–1289.CrossRefGoogle Scholar
Hedreen, J.C. (1998). What was wrong with the Abercrombie and empirical cell counting methods? A review. The Anatomical Record 250, 373–380.Google Scholar
Hefti, F. & Will, B. (1987). Nerve growth factor is a neurotrophic factor for forebrain cholinergic neurons; implications for Alzheimer’s disease. Journal of Neural Transmission, Supplement 24, 309–315.Google Scholar
Henderson, Z. (1987). Source of cholinergic input to ferret visual cortex. Brain Research 412, 261–268.Google Scholar
Ikonomovic, M.D., Mufson, E.J., Wuu, J., Bennett, D.A. & DeKosky, S.T. (2005). Reduction of choline acetyltransferase activity in primary visual cortex in mild to moderate Alzheimer’s disease. Archives of Neurology 62, 425–430.Google Scholar
Kang, J.I., Huppe-Gourgues, F. & Vaucher, E. (2014). Boosting visual cortex function and plasticity with acetylcholine to enhance visual perception. Frontiers in Systems Neuroscience 8, 172.CrossRefGoogle ScholarPubMed
Kirkwood, A., Rozas, C., Kirkwood, J., Perez, F. & Bear, M.F. (1999). Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. The Journal of Neuroscience 19, 1599–1609.Google Scholar
Klinkenberg, I., Sambeth, A. & Blokland, A. (2011). Acetylcholine and attention. Behavioural Brain Research 221, 430–442.CrossRefGoogle ScholarPubMed
Laplante, F., Morin, Y., Quirion, R. & Vaucher, E. (2005). Acetylcholine release is elicited in the visual cortex, but not in the prefrontal cortex, by patterned visual stimulation: A dual in vivo microdialysis study with functional correlates in the rat brain. Neuroscience 132, 501–510.Google Scholar
Lee, K.F., Li, E., Huber, L.J., Landis, S.C., Sharpe, A.H., Chao, M.V. & Jaenisch, R. (1992). Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69, 737–749.CrossRefGoogle ScholarPubMed
Minces, V.H., Alexander, A.S., Datlow, M., Alfonso, S.I. & Chiba, A.A. (2013). The role of visual cortex acetylcholine in learning to discriminate temporally modulated visual stimuli. Frontiers in Behavioral Neuroscience 7, 16.Google Scholar
Naumann, T., Casademunt, E., Hollerbach, E., Hofmann, J., Dechant, G., Frotscher, M. & Barde, Y.A. (2002). Complete deletion of the neurotrophin receptor p75NTR leads to long-lasting increases in the number of basal forebrain cholinergic neurons. The Journal of Neuroscience 22, 2409–2418.CrossRefGoogle ScholarPubMed
Niewiadomska, G., Mietelska-Porowska, A. & Mazurkiewicz, M. (2011). The cholinergic system, nerve growth factor and the cytoskeleton. Behavioural Brain Research 221, 515–526.CrossRefGoogle ScholarPubMed
Nilsson, O.G., Leanza, G., Rosenblad, C., Lappi, D.A., Wiley, R.G. & Bjorklund, A. (1992). Spatial learning impairments in rats with selective immunolesion of the forebrain cholinergic system. Neuroreport 3, 1005–1008.Google Scholar
Origlia, N., Kuczewski, N., Aztiria, E., Gautam, D., Wess, J. & Domenici, L. (2006). Muscarinic acetylcholine receptor knockout mice show distinct synaptic plasticity impairments in the visual cortex. The Journal of Physiology 577, 829–840.CrossRefGoogle ScholarPubMed
Paul, C.E., Vereker, E., Dickson, K.M. & Barker, P.A. (2004). A pro-apoptotic fragment of the p75 neurotrophin receptor is expressed in p75NTRExonIV null mice. The Journal of Neuroscience 24, 1917–1923.Google Scholar
Pioro, E.P. & Cuello, A.C. (1990). Distribution of nerve growth factor receptor-like immunoreactivity in the adult rat central nervous system. Effect of colchicine and correlation with the cholinergic system–I. Forebrain. Neuroscience 34, 57–87.Google Scholar
Poort, J., Khan, A.G., Pachitariu, M., Nemri, A., Orsolic, I., Krupic, J., Bauza, M., Sahani, M., Keller, G.B., Mrsic-Flogel, T.D. & Hofer, S.B. (2015). Learning enhances sensory and multiple non-sensory representations in primary visual cortex. Neuron 86, 1478–1490.Google Scholar
Ridley, R.M., Pugh, P., Maclean, C.J. & Baker, H.F. (1999). Severe learning impairment caused by combined immunotoxic lesion of the cholinergic projections to the cortex and hippocampus in monkeys. Brain Research 836, 120–138.Google Scholar
Rossi, F.M., Sala, R. & Maffei, L. (2002). Expression of the nerve growth factor receptors TrkA and p75NTR in the visual cortex of the rat: Development and regulation by the cholinergic input. The Journal of Neuroscience 22, 912–919.Google Scholar
Sanchez-Ortiz, E., Yui, D., Song, D., Li, Y., Rubenstein, J.L., Reichardt, L.F. & Parada, L.F. (2012). TrkA gene ablation in basal forebrain results in dysfunction of the cholinergic circuitry. The Journal of Neuroscience 32, 4065–4079.Google Scholar
Siciliano, R., Fornai, F., Bonaccorsi, I., Domenici, L. & Bagnoli, P. (1999). Cholinergic and noradrenergic afferents influence the functional properties of the postnatal visual cortex in rats. Visual Neuroscience 16, 1015–1028.CrossRefGoogle ScholarPubMed
Sobreviela, T., Clary, D.O., Reichardt, L.F., Brandabur, M.M., Kordower, J.H. & Mufson, E.J. (1994). TrkA-immunoreactive profiles in the central nervous system: Colocalization with neurons containing p75 nerve growth factor receptor, choline acetyltransferase, and serotonin. Journal of Comparative Neurology 350, 587–611.Google Scholar
von Bohlen und Halbach, O. (2013). Analysis of morphological changes as a key method in studying psychiatric animal models. Cell & Tissue Research 354, 41–50.Google Scholar
von Bohlen und Halbach, O., Minichiello, L. & Unsicker, K. (2005). Haploinsufficiency for trkB and trkC receptors induces cell loss and accumulation of alpha-synuclein in the substantia nigra. FASEB Journal 19, 1740–1742.Google Scholar
von Bohlen und Halbach, O. & Unsicker, K. (2003). Age-related decline in the tyrosine hydroxylase-immunoreactive innervation of the amygdala and dentate gyrus in mice. Cell & Tissue Research 311, 139–143.Google Scholar
von Schack, D., Casademunt, E., Schweigreiter, R., Meyer, M., Bibel, M. & Dechant, G. (2001). Complete ablation of the neurotrophin receptor p75NTR causes defects both in the nervous and the vascular system. Nature Neuroscience 4, 977–978.Google Scholar
Yeo, T.T., Chua-Couzens, J., Butcher, L.L., Bredesen, D.E., Cooper, J.D., Valletta, J.S., Mobley, W.C. & Longo, F.M. (1997). Absence of p75NTR causes increased basal forebrain cholinergic neuron size, choline acetyltransferase activity, and target innervation. The Journal of Neuroscience 17, 7594–7605.CrossRefGoogle ScholarPubMed