High serotonin levels during brain development alter the structural input-output connectivity of neural networks in the rat somatosensory layer IV

Frontiers in Cellular Neuroscience

Volumn , Issue MAY, 2013, Pages

  Miceli, Stéphanie ^a   Negwer, Moritz ^a   van Eijs, Fenneke ^a   Kalkhoven, Carla ^a   van Lierop, Ilja ^a   Homberg, Judith ^a   Schubert, Dirk ^a  

^a RADBOUD UNIVERSITY   (Netherlands)

Author keywords

Barrel cortex; Columnar circuitry; Electrophysiology; Morphology; Pyramidal cell; Serotonin; SERT; Somatosensory; Spiny stellate cell

Indexed keywords

SEROTONIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN REGION; CELL POPULATION; CELL STRUCTURE; CONTROLLED STUDY; MALE; NERVE CELL NETWORK; NERVE CELL STIMULATION; NERVE FIBER; NONHUMAN; PYRAMIDAL NERVE CELL; RAT; SEROTONIN BRAIN LEVEL; SOMATOSENSORY CORTEX; SOMATOSENSORY SYSTEM; SYNAPTIC TRANSMISSION; THALAMOCORTICAL TRACT; THALAMUS; THALAMUS NUCLEUS;

EID: 84878286221     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00088     Document Type: Article

References (90)

1. Agmon, A., and Connors, B. W., (1991). Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41, 365-379.
2. Alloway, K. D., Zhang, M., and Chakrabarti, S. (2004). Septal columns in rodent barrel cortex: functional circuits for modulating whisking behavior. The Journal of Comparative Neurology 480, 299-309.
3. Bender, K. J., Rangel, J., and Feldman, D. (2003). Development of columnar topography in the excitatory layer 4 to layer 2/3 projection in rat barrel cortex. The Journal of Neuroscience 23, 8759-70.
4. Bennett-Clarke, C. A., Chiaia, N.L., and Rhoades, R. W. (1996). Thalamocortical afferents in rat transiently express high-affinity serotonin uptake sites. Brain Research 733, 301-6.
5. Blakely, R. D., Berson, H. E., Fremeau, R. T., Caron, M. G., Peek, M. M., Prince, H. K., and Bradley, C. C. (1991). Cloning and expression of functional serotonin transporter from rat brain. Nature 354, 66-70.
6. Bonnin, A., Torii, M., Wang, L., Rakic, P., and Levitt, P. (2007). Serotonin modulates the response of embryonic thalamocortical axons to Netrin-1. Nature Neuroscience 10, 588-97.
7. Bonnin, A., Zhang, L., Blakely, R. D., and Levitt, P. (2012). The SSRI citalopram affects fetal thalamic axon responsiveness to netrin-1 in vitro independently of SERT antagonism. Neuropsychopharmacology 37, 1879-1884.
8. Bou-Flores, C., Lajard, A. M., Monteau, R., De Maeyer, E., Seif, I., Lanoir, J., and Hilaire, H., (2000). Abnormal phrenic motoneuron activity and morphology in neonatal monoamine oxidase A-deficient transgenic mice: possible role of a serotonin excess. The Journal of Neuroscience 20, 4646-56.
9. Brecht, M., (2007). Barrel cortex and whisker-mediated behaviors. Current Opinion in Neurobiology 17, 408-16.
10. Brecht, M., Schneider, M., Sakmann, B., and Margrie, T. W. (2004). Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 427, 704-10.
11. Bureau I, von Saint Paul F, Svoboda K. (2006). Interdigitated paralemniscal and lemniscal pathways in the mouse barrel cortex. PLoS Biol, 4, e382.
12. Callaway, E. M., and Katz, L. C. (1992). Development of axonal arbors of layer 4 spiny neurons in cat striate cortex. The Journal of Neuroscience 12:570-582.
13. Callaway, E. M., and Wiser, A. K. (1996). Contributions of individual layer 2-5 spiny neurons to local circuits in macaque primary visual cortex. Visual Neuroscience 13, 907-22.
14. Callaway, E. M., and Borrell, V. (2011). Developmental sculpting of dendritic morphology of layer 4 neurons in visual cortex: influence of retinal input. The Journal of Neuroscience 31, 7456-70.
15. Canli, T., and Lesch, K. P., (2007). Long story short: the serotonin transporter in emotion regulation and social cognition. Nature Neuroscience 10, 1103-9.
16. Cases, O, Vitalis, T., Seif, I., De Maeyer, E., Sotelo, C., and Gaspar, P. (1996). Lack of barrels in the somatosensory cortex of monoamine oxidase A-deficient mice: role of a serotonin excess during the critical period. Neuron 16, 297-307.
17. Chagnac-Amitai, Y., and Connors, B. W. (1989). Horizontal spread of synchroized activity in neocortex and its control by GABA-mediated inhibition. Journal Neurophysiology 61, 747-58.
18. Champoux, M., Bennett, A., Shannon, C., Higley, J. D., Lesch, K. P., and Suomi, S.J. (2002). Serotonin transporter gene polymorphism, differential early rearing, and behavior in rhesus monkey neonates. Molecular Psychiatry 7, 1058-63.
19. Connors, B. W., and Gutnick, M. J. (1990). Intrinsic firing patterns of diverse neocortical neurons. Trends in Neuroscience 13, 99-104.
20. Cruikshank, S. J., Lewis, T. J., and Connors, B. W. (2007). Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nature Neuroscience 10, 462-8.
21. Datwani, A. (2002). NMDA receptor-dependent pattern transfer from afferents to postsynaptic cells and dendritic differentiation in the barrel cortex. Molecular and Cellular Neuroscience 21, 477-492.
22. Daubert, E. A., and Condron, B. J. (2011). Serotonin: a regulator of neuronal morphology and circuitry. 33, 424-434.
23. Derkach, V. A., Oh, M. C., Guire, E. S., and Soderling, T. R. (2007). Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat. Rev. Neurosci. 8, 101-113.
24. Diamond, M. E. (1995). Somatosensory thalamus of the rat. In: Jones E.G., Diamond, IT (eds) The barrel cortex of rodents. Plenum Press, New York, 189-219.
25. Douglas, R. J., and Martin, K. A. C. (2004). Neuronal circuits of the neocortex. Annual Review of Neuroscience 27, 419-51.
26. Erzurumlu, R. S., and Kind, P. C. (2001). Neural activity: sculptor of 'barrels' in the neocortex. Trends in Neurosciences 24, 589-95.
27. Esaki, T., Cook, M., Shimoji, K., Murphy, D. L., Sokoloff, L., and Holmes, A. (2005). Developmental disruption of serotonin transporter function impairs cerebral responses to whisker stimulation in mice. Proceedings of the National Academy of Sciences of the United States of America 102, 5582-7.
28. Feldman, D. E. (2000). Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 27, 45-56.
29. Feldman, D. E., Nicoll, R. A., and Malenka, R. C. (1999). Synaptic plasticity at thalamocortical synapses in developing rat somatosensory cortex: LTP, LTD, and silent synapses. Journal of Neurobiology 41, 92-101.
30. Feldmeyer, D., Egger, V., Lubke, J., and Sakmann, B. (1999). Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single 'barrel' of developing rat somatosensory cortex. The Journal of Physiology 521, 169-90.
31. Feldmeyer, D. (2012). Excitatory neuronal connectivity in the barrel cortex. Frontiers in Neuroanatomy 6, 24.
32. Feldmeyer, D., Brecht, M., Helmchen, F., Petersen, C. C., Poulet, J. F. A., Staiger, J. F., Luhmann, H.J., and Schwarz, C. (2013). Barrel cortex function. Progress in Neurobiology 26.
33. Feldmeyer, D., Lübke, J., Silver, R. A., and Sakmann, B. (2002). Synaptic connections between layer 4 spiny neurone - layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column. Journal of Physiology 538, 803-822.
34. Foehring, R. C., van Brederode, J. F. M., Kinney, G. A., and Spain, W.J. (2002). Serotonergic modulation of supragranular neurons in rat sensorimotor cortex. The Journal of Neuroscience 22, 8238-8250.
35. Fox, K. (2002). Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex. Neuroscience 111, 799-814.
36. Gabernet, L., Jadhav, S. P., Feldman, D. E., Carandini, M., and Scanziani, M. (2005). Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. Neuron 48, 315-27.
37. Gaspar, P., Cases, O., and Maroteaux, L. (2003). The developmental role of serotonin: news from mouse molecular genetics. Nature reviews. Neuroscience 4, 1002-12.
38. Gilbert, D. and Wiesel, T. N. (1983). Clustered intrinsic connections in cat visual cortex. Journal Neuroscience 3, 1116-1133.
39. Gonzales-Burgos, I., del Angel-Meza, A. R., Barajas-Lopez, G., and Feria-Velasco, A. (1996). Tryptophan restriction causes long-term plastic changes in corticofrontal pyramidal neurons. International Journal of Developmental Neuroscience 14, 673-9.
40. Harris, R. M., and Woolsey, T. A. (1983). Computer-assisted analyses of barrel neuron axons and their putative synaptic targets. J. Comp. Neurol 220, 63-79.
41. Hayashi, T., Ohtani, A., Onuki, F., Natsume, M., Li, F., Satou, T., Yoshikawa, M., Senzaki, K., Shiga, T. (2010). Roles of serotonin 5-HT 3 receptor in the formation of dendrites and axons in the rat cerebral cortex: An in vitro study. Neuroscience Research 66, 22-29.
42. Homberg, J. R., Olivier, J. D. A., and Smits, B. M. G. (2007). Characterization of the serotonin transporter knockout rat: a selective change in the functioning of the serotonergic system Neuroscience 146, 1662-1676.
43. Homberg, J. R, Schubert, D., and Gaspar, P. (2010). New perspectives on the neurodevelopmental effects of SSRIs. Trends in pharmacological sciences 31, 60-5.
44. Jensen K. F. and Killackey H. P. (1987). Terminal arbors of axons projecting to the somatosensory cortex of the adult rat. I. The normal morphology of specific thalamocortical afferents. The Journal of Neuroscience 7, 3529-3543.
45. Jitsuki, S., Takemoto, K., Kawasaki, T., Tada, H., Takahashi, A., Becamel, C., Sano, A., Yuzaki, M., Zukin, R.S., Ziff, E.B., et al. (2011). Serotonin mediates cross-modal reorganization of cortical circuits. Neuron 69, 780-792.
46. Kimura, F., Itami, C., Ikezoe, K., Tamura, H., Fujita, I., Yanagawa, Y., Obata, K., Ohshima, M. (2010). Fast activation of feedforward inhibitory neurons from thalamic input and its relevance to the regulation of spike sequences in the barrel cortex. The Journal of physiology, 588, 2769-87.
47. King, M. A., Louis, P. M., Hunter, B. E., and Walker, D. W. (1989). Biocytin: a versatile anterograde neuroanatomical tract-tracing alternative. Brain research, 497, 361-7.
48. Land, P. W., and Kandler, K. (2002). Somatotopic organization of rat thalamocortical slices. Journal of Neuroscience Methods 119, 15-21.
49. Laurent, A., Goaillard, J.-M., Cases, O., Lebrand, C., Gaspar, P., and Ropert, N. (2002). Activity-dependent presynaptic effect of serotonin 1B receptors on the somatosensory thalamocortical transmission in neonatal mice. The Journal of Neuroscience 22, 886-900.
50. Lebrand, C., Blakely, R. D., Cases, O., Wehrle, R., Edwards, R. H., Gaspar, P. (1998). Transient developmental expression of monoamine transporters in the rodent forebrain, 524, 506-524.
51. Lebrand, C., Cases, O., Adelbrecht, C., Doye, A., Alvarez, C., El Mestikawy, S., Seif, I., Gaspar, P. (1996). Transient uptake and storage of serotonin in developing thalamic neurons. Neuron 17, 823-35.
52. Lee, L.-J. (2009). Neonatal fluoxetine exposure affects the neuronal structure in the somatosensory cortex and somatosensory-related behaviors in adolescent rats. Neurotoxicity research 15, 212-23.
53. Lee, L.-J., and Lee, L. J.-H. (2012). Neonatal fluoxetine exposure alters motor performances of adolescent rats. Developmental neurobiology 72, 1122-32.
54. Lesch, K. P., Bengel, D., Heils, A., Sabol, S. Z., Greenberg, B. D., Petri, S., Benjamin, J., Mueller, C. R., Hamer, D. H., Murphy, D. L. (1996). Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274, 1527-31.
55. Lesch K. P., Waider J. (2012). Serotonin in the modulation of neural plasticity and networks: implications for neurodevelopmental disorders. Neuron 76, 175-191.
56. Levitt, P., Harvey, J. A, Friedman, E., Simansky, K., and Murphy, E. H. (1997). New evidence for neurotransmitter influences on brain development. Trends in neurosciences 20, 269-74.
57. Li, H., and Crair, M. C. (2011). How do barrels form in somatosensory cortex? Annals of the New York Academy of Sciences 1225, 119-129.
58. López-Bendito, G., and Molnár, Z. (2003). Thalamocortical development: how are we going to get there? Nature reviews. Neuroscience, 4, 276-89.
59. Lübke, J, Egger, V., Sakmann, B., and Feldmeyer, D. (2000). Columnar organization of dendrites and axons of single and synaptically coupled excitatory spiny neurons in layer 4 of the rat barrel cortex. The Journal of neuroscience 20, 5300-11.
60. Lübke, Joachim, and Feldmeyer, D. (2007). Excitatory signal flow and connectivity in a cortical column: focus on barrel cortex. Brain structure and function, 212, 3-17.
61. Makino, H., and Malinow, R. (2009). AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron 64, 381-390.
62. Meyer H. S., Wimmer V. C., Hemberger M, Bruno R. M., de Kock C. P., Frick A, Sakmann B, Helmstaedter M. (2010). Cell type-specific thalamic innervation in a column of rat vibrissal cortex. Cereb Cortex 20, 2287-2303.
63. Narboux-Neme, N., Evrard, a., Ferezou, I., Erzurumlu, R. S., Kaeser, P. S., Laine, J., Rossier, J., Ropert, N., Suedhof, T. C., and Gaspar, P. (2012). Neurotransmitter release at the thalamocortical synapse instructs barrel formation but not axon patterning in the somatosensory cortex. Journal of Neuroscience 32, 6183-6196.
64. Norrholm, S. D., and Ouimet, C. C. (2000). Chronic fluoxetine administration to juvenile rats prevents age-associated dendritic spine proliferation in hippocampus. Brain research 883, 205-15.
65. Oberlaender, M., De Kock, C. P. J., Bruno, R. M., Ramirez, A., Meyer, H. S., Dercksen, V. J., Helmstaedter, M., Sakmann, B. (2012). Cell type-specific three-dimensional structure of thalamocortical circuits in a column of rat vibrissal cortex. Cerebral cortex 22, 2375-91.
66. Oberlaender, M., Ramirez, A., & Bruno, R. M. (2012). Sensory experience restructures thalamocortical axons during adulthood. Neuron 74, 648-55.
67. Olivier, J. D. A, Van Der Hart, M. G. C., Van Swelm, R. P. L., Dederen, P. J., Homberg, J. R., Cremers, T., Deen, P. M. T., Cuppen, E., Cools, A. R., Ellenbroek, B. A. (2008). A study in male and female 5-HT transporter knockout rats: an animal model for anxiety and depression disorders. Neuroscience, 152, 573-84.
68. Pang, R. D., Wang, Z., Klosinski, L. P., Guo, Y., Herman, D. H., Celikel, T., Dong, H. W., Holschneider, D. P. (2011). Mapping functional brain activation using [C]- iodoantipyrine in male serotonin transporter knockout mice. PloS One 6, p. e23869.
69. Persico, A. M., Mengual, E., Moessner, R., Hall, F. S., Revay, R. S., Sora, I., Arellano, J., DeFelipe, J., Gimenez-Amaya, J. M., Conciatory, M., Marino, R., Baldi, A., Cabib, S., Pascucci, T., Uhl, G. R., Murphy, D. L., Lesch, K. P., Keller, F. (2001). Barrel pattern formation requires serotonin uptake by thalamocortical afferents, and not vesicular monoamine release. The Journal of neuroscience 21, 6862-73.
70. Petersen, C. C. (2003). The barrel cortex--integrating molecular, cellular and systems physiology. European journal of physiology 447, 126-34.
71. Petersen, C. C. (2007). The functional organization of the barrel cortex. Neuron 56, 339-55.
72. Petersen, C. C., and Sakmann, B. (2000). The excitatory neuronal network of rat layer 4 barrel cortex. The Journal of neuroscience 20, 7579-86.
73. Rebsam, A., Seif, I., & Gaspar, P. (2002). Refinement of thalamocortical arbors and emergence of barrel domains in the primary somatosensory cortex: a study of normal and monoamine oxidase a knock-out mice. The Journal of neuroscience 22, 541-52.
74. Riccio, O., Jacobshagen, M., Golding, B., Vutskits, L., Jabaudon, D., Hornung, J.P., and Dayer, A.G. (2011). Excess of serotonin affects neocortical pyramidal neuron migration. Translational Psychiatry 1, e47.
75. Salichon, N., Gaspar, P., Upton, A.L., Picaud, S., Hanoun, N., Hamon, M., De Maeyer, E., Murphy, D.L., Mössner, R., Lesch, K.P., Hen, R., and Seif, I. (2001). Excessive activation of serotonin (5-HT) 1B receptors disrupts the formation of sensory maps in monoamine oxidase A and 5-HT transporter knock-out mice. The Journal of Neuroscience 21, 884-896.
76. Schmitz, D., Empson, R.M., Gloveli, T., and Heinemann, U. (1995). Serotonin reduces synaptic excitation of principal cells in the superficial layers of rat hippocampalentorhinal cortex combined slices. Neuroscience Letters 190, 37-40.
77. Schubert, D., Staiger, J.F., Cho, N., Kötter, R., Zilles, K., and Luhmann, H.J. (2001). Layer-specific intracolumnar and transcolumnar functional connectivity of layer V pyramidal cells in rat barrel cortex. The Journal of Neuroscience 21, 3580-3592.
78. Schubert, D., Kötter, R., and Staiger, J.F. (2007). Mapping functional connectivity in barrel-related columns reveals layer-and cell type-specific microcircuits. Brain Structure & Function 212, 107-119.
79. Schubert, D., Kötter, R., Zilles, K., Luhmann, H.J., and Staiger, J.F. (2003). Cell type-specific circuits of cortical layer IV spiny neurons. The Journal of Neuroscience 23, 2961-2970.
80. Shepherd, G.M.G., Stepanyants, A., Bureau, I., Chklovskii, D., and Svoboda, K. (2005). Geometric and functional organization of cortical circuits. Nature Neuroscience 8, 782-790.
81. Smits, B.M.G., Mudde, J.B., van de Belt, J., Verheul, M., Olivier, J., Homberg, J., Guryev, V., Cools, A.R., Ellenbroek, B.A., Plasterk, R.H.A., and Cuppen, E. (2006). Generation of gene knockouts and mutant models in the laboratory rat by ENU-driven target-selected mutagenesis. Pharmacogenetics and Genomics 16, 159-169.
82. Staiger, J.F., Zilles, K., and Freund, T.F. (1996). Recurrent axon collaterals of corticothalamic projection neurons in rat primary somatosensory cortex contribute to excitatory and inhibitory feedback-loops. Anatomy and Embryology 194, 533-543.
83. Staiger, J.F., Flagmeyer, I., Schubert, D., Zilles, K., Kötter, R., and Luhmann, H.J. (2004). Functional diversity of layer IV spiny neurons in rat somatosensory cortex: quantitative morphology of electrophysiologically characterized and biocytin labeled cells. Cerebral Cortex 14, 690-701.
84. Stratford, K.J, Tarcy-Hornoch, K., Martin, K.A.C., Bannister, N.J., and Jack J.J.B. (1996). Excitatory synaptic inputs to spiny stellate cells in cat visual cortex. Letters to Nature 382, 258-261.
85. Sun, Q.Q., Huguenard J.R., and Prince D.A. (2006). Barrel cortex microcircuits: thalamocortical feedforward inhibition in spiny stellate cells is mediated by a small number of fast-spiking interneurons. The Journal of Neuroscience 26, 1219-1230.
86. Varga, Z., Jia, H., Sakmann, B., and Konnerth, A. (2011). Dendritic coding of multiple sensory inputs in single cortical neurons in vivo. Proceedings of the National Academy of Sciences USA 108, 15420-15425.
87. Waterhouse, B.D., Moises, H.C., and Woodward, D.J. (1986). Interaction of serotonin with somatosensory cortical neuronal responses to afferent synaptic inputs and putative neurotransmitters. Brain Research Bulletin 17, 507-518.
88. Wellman, C.L., Izquierdo, A., Garrett, J.E., Martin, K.P., Carroll, J., Millstein, R., Lesch, K.P., Murphy, D.L., and Holmes, A. (2007). Impaired stress-coping and fear extinction and abnormal corticolimbic morphology in serotonin transporter knock-out mice. The Journal of Neuroscience 27, 684-691.
89. Woolsey, T.A., and Van der Loos, H. (1970). The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Research 17, 205-242.
90. Xu, Y., Sari, Y., and Zhou, F.C. (2004). Selective serotonin reuptake inhibitor disrupts organization of thalamocortical somatosensory barrels during development. Brain Research. Developmental Brain Research 150, 151-161.