Hippocampal subfield-specific Homer1a expression is triggered by learning-facilitated long-term potentiation and long-term depression at medial perforant path synapses.


Journal

Hippocampus
ISSN: 1098-1063
Titre abrégé: Hippocampus
Pays: United States
ID NLM: 9108167

Informations de publication

Date de publication:
08 2021
Historique:
revised: 22 03 2021
received: 05 10 2020
accepted: 11 04 2021
pubmed: 9 5 2021
medline: 25 2 2022
entrez: 8 5 2021
Statut: ppublish

Résumé

Learning about general aspects, or content details, of space results in differentiated neuronal information encoding within the proximodistal axis of the hippocampus. These processes are tightly linked to long-term potentiation (LTP) and long-term depression (LTD). Here, we explored the precise sites of encoding of synaptic plasticity in the hippocampus that are mediated by information throughput from the perforant path. We assessed nuclear Homer1a-expression that was triggered by electrophysiological induction of short and long forms of hippocampal synaptic plasticity, and compared it to Homer1a-expression that was triggered by LTP and LTD enabled by different forms of spatial learning. Plasticity responses were induced by patterned stimulation of the perforant path and were recorded in the dentate gyrus (DG) of freely behaving rats. We used fluorescence in situ hybridization to detect experience-dependent nuclear encoding of Homer1a in proximodistal hippocampal subfields. Induction of neither STP nor STD resulted in immediate early gene (IEG) encoding. Electrophysiological induction of robust LTP, or LTD, resulted in highly significant and widespread induction of nuclear Homer1a in all hippocampal subfields. LTP that was facilitated by novel spatial exploration triggered similar widespread Homer1a-expression. The coupling of synaptic depression with the exploration of a novel configuration of landmarks resulted in localized IEG expression in the proximal CA3 region and the lower (infrapyramidal) blade of the DG. Our findings support that synaptic plasticity induction via perforant path inputs promotes widespread hippocampal information encoding. Furthermore, novel spatial exploration promotes the selection of a hippocampal neuronal network by means of LTP that is distributed in an experience-dependent manner across all hippocampus subfields. This network may be modified during spatial content learning by LTD in specific hippocampal subfields. Thus, long-term plasticity-inducing events result in IEG expression that supports establishment and/or restructuring of neuronal networks that are necessary for long-term information storage.

Identifiants

pubmed: 33964041
doi: 10.1002/hipo.23333
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

897-915

Informations de copyright

© 2021 The Authors. Hippocampus published by Wiley Periodicals LLC.

Références

Abraham, W. C., Dragunow, M., & Tate, W. P. (1991). The role of immediate early genes in the stabilization of long-term potentiation. Molecular Neurobiology, 5, 297-314.
Abraham, W. C., & Williams, J. M. (2008). LTP maintenance and its protein synthesis-dependence. Neurobiology of Learning and Memory, 89, 260-268.
Alberini, C. M., Ghirardl, M., Metz R., & Kandel, E. R. (1994). C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell, 76, 1099-1114.
Amaral, D. G., Scharfman, H. E., & Lavenex, P. (2007). The dentate gyrus: Fundamental neuroanatomical organization (dentate gyrus for dummies). Progress in Brain Research, 163, 3-22.
André, M. A. E., & Manahan-Vaughan, D. (2013). Spatial olfactory learning facilitates long-term depression in the hippocampus. Hippocampus, 23, 963-968.
Bartsch, D., Ghirardi, M., Skehel, P. A., Karl, K. A., Herder, S. P., Chen, M., Bailey C. H., & Kandel, E. R. (1995). Aplysia CREB2 represses long-term facilitation: Relief of repression converts transient facilitation into long-term functional and structural change. Cell, 83, 979-992.
Bilkey, D. K., Cheyne, K. R., Eckert, M. J., Lu, X., Chowdhury, S., Worley, P. F., … Abraham, W. C. (2017). Exposure to complex environments results in more sparse representations of space in the hippocampus. Hippocampus, 27, 1178-1191.
Bliss, T. V., & Lomo, T. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. Journal of Physiology (London), 232, 331-356.
Brakeman, P. R., Lanahan, A. A., O'Brien, R., Roche, K., Barnes, C. A., Huganir, R. L., & Worley, P. F. (1997). Homer: A protein that selectively binds metabotrophic glutamate receptors. Nature, 386, 284-288.
Bromer, C., Bartol, T. M., Bowden, J. B., Hubbard, D. D., Hanka, D. C., Gonzalez, P. V., … Harris, K. M. (2018). Long-term potentiation expands information content of hippocampal dentate gyrus synapses. Proceedings of the National Academy of Sciences of the USA, 115, E2410-E2418.
Byrne, J. H., Zwartjes, R., Homayouni, R., Critz, S. D., & Eskin, A. (1993). Roles of second messenger pathways in neuronal plasticity and in learning and memory. Insights gained from Aplysia. Advances in Second Messenger and Phosphoprotein Research, 27, 47-108.
Castellucci, V. F., Kandel, E. R., Schwartz, J. H., Wilson, F. D., Nairn, A. C., & Greengard, P. (1980). Intracellular injection of the catalytic subunit of cyclic AMP-dependent protein kinase simulates facilitation of transmitter release underlying behavioral sensitization in Aplysia. Proceedings of the National Academy of Sciences of the USA, 77, 7492-7496.
Chawla, M. K., Guzowski, J. F., Ramirez-Amaya, V., Lipa, P., Hoffman, K. L., Marriott, L. K., … Barnes, C. A. (2005). Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus, 15, 579-586.
Claiborne, B. J., Amaral, D. G., & Cowan, W. M. (1986). A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus. The Journal of Comparative Neurology, 246, 435-458.
Clifton, N. E., Trent, S., Thomas, K. L., & Hall, J. (2019). Regulation and function of activity-dependent Homer in synaptic plasticity. Mol Neuropsychiatry, 5, 147-161.
Cole, A. J., Abu-Shakra, S., Saffen, D. W., Baraban, J. M., & Worley, P. F. (1990). Rapid rise in transcription factor mRNAs in rat brain after electroshock-induced seizures. Journal of Neurochemistry, 55, 1920-1927.
Cole, A. J., Saffen, D. W., Baraban, J. M., & Worley, P. F. (1989). Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature, 340, 474-476.
Dash, P. K., Hochner, B., & Kandel, E. R. (1990). Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature, 345, 718-721.
Daumas, S., Halley, H., Francés, B., & Lassalle, J.-M. (2005). Encoding, consolidation, and retrieval of contextual memory: Differential involvement of dorsal CA3 and CA1 hippocampal subregions. Learning and Memory, 12, 375-382.
Deshmukh, S. S., & Knierim, J. J. (2011). Representation of non-spatial and spatial information in the lateral Entorhinal cortex. Frontiers in Behavioral Neuroscience, 5, 69.
Dietz, B., & Manahan-Vaughan, D. (2017). Hippocampal long-term depression is facilitated by the acquisition and updating of memory of spatial auditory content and requires mGlu5 activation. Neuropharmacology, 115, 30-41.
Dudek, S. M., & Bear, M. F. (1992). Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci USA, 89, 4363-4367.
Ferbinteanu, J., Holsinger, R. M. D., & McDonald, R. J. (1999). Lesions of the medial or lateral perforant path have different effects on hippocampal contributions to place learning and on fear conditioning to context. Behavioural Brain Research, 101, 65-84.
Flasbeck, V., Atucha, E., Nakamura, N. H., Yoshida, M., & Sauvage, M. M. (2018). Spatial information is preferentially processed by the distal part of CA3: Implication for memory retrieval. Behavioural Brain Research, 354, 31-38.
Frey, U., & Morris, R. G. (1997). Synaptic tagging and long-term potentiation. Nature, 385, 533-536.
Garner, A. R., Rowland, D. C., Hwang, S. Y., Baumgaertel, K., Roth, B. L., Kentros, C., & Mayford, M. (2012). Generation of a synthetic memory trace. Science, 335, 1513-1516.
Genzel, L., Schut, E., Schröder, T., Eichler, R., Khamassi, M., Gomez, A., … Battaglia, F. (2019). The object space task shows cumulative memory expression in both mice and rats. PLoS Biology, 17, e3000322.
Guzowski, J. F., Mc Naughton, B. L., Barnes, C. A., & Worley, P. F. (1999). Environment-specific expression of the immediate-early gene arc in hippocampal neuronal ensembles. Nature, 2, 1120-1124.
Guzowski, J.F., & Worley, P.F. (2001) Cellular compartment analysis of temporal activity by fluorescence in situ hybridization (catFISH). Current Protocols in Neuroscience Chapter 1:Unit 1.8.
Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., & Moser, E. I. (2005). Microstructure of a spatial map in the entorhinal cortex. Nature, 436, 801-806.
Hagena, H., & Manahan-Vaughan, D. (2011). Learning-facilitated synaptic plasticity at CA3 mossy fiber and commissural-associational synapses reveals different roles in information processing. Cerebral Cortex, 21, 2442-2449.
Hagena, H., & Manahan-Vaughan, D. (2012). Learning-facilitated long-term depression and long-term potentiation at mossy fiber-CA3 synapses requires activation of β-adrenergic receptors. Frontiers in Integrative Neuroscience, 6, 1-11.
Hagena, H., & Manahan-Vaughan, D. (2013). Differentiation in the protein synthesis-dependency of persistent synaptic plasticity in mossy fiber and associational/commissural CA3 synapses in vivo. Frontiers in Integrative Neuroscience, 7, 1-12.
Hall, J., Thomas, K. L., & Everitt, B. J. (2000). Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nature Neuroscience, 3, 533-535.
Hebb, D. O. (1949). Organization of behavior. New York: John Wiley & Sons.
Hennou, S., Kato, A., Schneider, E. M., Lundstrom, K., Gahwiler, B. H., Inokuchi, K., … Ehrengruber, M. U. (2003). Homer-1a/Vesl-1S enhances hippocampal synaptic transmission. European Journal of Neuroscience, 18, 811-819.
Hess, U. S., Lynch, G., & Gall, C. M. (1995a). Changes in c-fos mRNA expression in rat brain during odor discrimination learning: Differential involvement of hippocampal subfields CA1 and CA3. The Journal of Neurocience, 15, 4786-4795.
Hess, U. S., Lynch, G., & Gall, C. M. (1995b). Regional patterns of c-fos mRNA expression in rat hippocampus following exploration of a novel environment versus performance of a well-learned discrimination. The Journal of Neurocience, 15, 7796-7809.
Hjorth-Simonsen, A., & Jeune, B. (1972). Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation. The Journal of Comparative Neurology, 144, 215-232.
Hoang, T.-H., Aliane, V., & Manahan-Vaughan, D. (2018). Novel encoding and updating of positional, or directional, spatial cues are processed by distinct hippocampal subfields: Evidence for parallel information processing and the "what" stream. Hippocampus, 28, 315-326.
Huang, Y. Y., & Kandel, E. R. (1994). Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization. Learning and Memory, 1, 74-82.
Ishizuka, N., Weber, J., & Amaral, D. G. (1990). Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. The Journal of Comparative Neurology, 295, 580-623.
Ito, H. T., & Schuman, E. M. (2012). Functional division of hippocampal area CA1 via modulatory gating of entorhinal cortical inputs. Hippocampus, 22, 372-387.
Jones, M. W., Errington, M. L., French, P. J., Fine, A., Bliss, T. V., Garel, S., … Davis, S. (2001). A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nature Neuroscience, 4, 289-296.
Kajiwara, R., Wouterlood, F. G., Sah, A., Boekel, A. J., Baks-te Bulte, L. T. G., & Witter, M. P. (2008). Convergence of entorhinal and CA3 inputs onto pyramidal neurons and interneurons in hippocampal area CA1-An anatomical study in the rat. Hippocampus, 18, 266-280.
Kandel, E. R., Dudai, Y., & Mayford, M. R. (2014). The molecular and systems biology of memory. Cell, 157, 163-186.
Kato A., Ozawa, F., Saitoh, Y., Fukazawa, Y., Sugiyama, H., & Inokuchi, K .(1998) Novel members of the Vesl/Homer family of PDZ proteins that bind metabotropic glutamate receptors. The Journal of Biological Chemistry 273, 23969-23975.
Kato, A., Ozawa, F., Saitoh, Y., Hirai, K., & Inokuchi, K. (1997). Vesl, a gene encoding VASP/Ena family related protein, is upregulated during seizure, long-term potentiation and synaptogenesis 1. FEBS Letters, 412, 183-189.
Kemp, A., & Manahan-Vaughan, D. (2004). Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proceedings of the National Academy of Sciences of the USA, 101, 8192-8197.
Kemp, A., & Manahan-Vaughan, D. (2007). Hippocampal long-term depression: Master or minion in declarative memory processes? Trends in Neurosciences, 30, 111-118.
Kemp, A., & Manahan-Vaughan, D. (2008). The hippocampal CA1 region and dentate gyrus differentiate between environmental and spatial feature encoding through long-term depression. Cerebral Cortex, 18, 968-977.
Kemp, A., Tischmeyer, W., & Manahan-Vaughan, D. (2013). Learning-facilitated long-term depression requires activation of the immediate early gene, c-fos, and is transcription dependent. Behavioural Brain Research, 254, 83-91.
Konorski, J. (1948). Conditioned reflexes and neuron organization. New York, NY: Cambridge University Press.
Lanahan, A. A., & Worley, P. F. (1998). Immediate-early genes and synaptic function. Neurobiology of Learning and Memory, 70, 37-43.
Manahan-Vaughan, D. (2018a). Recording field potentials and synaptic plasticity from freely behaving rodents. In Handbook of in vivo neural plasticity techniques, a systems neuroscience approach to the neural basis of memory and cognition. London: Academic Press. doi.org/10.1016/B978-0-12-812028-6.00001-X
Manahan-Vaughan, D. (2018b). Item encoding through hippocampal long-term potentiation and long-term depression. In A. Ennaceur & M. A. de Souza Silva (Eds.), Handbook of object novelty recognition. London, UK: Academic Press.
Manahan-Vaughan, D., & Braunewell, K. H. (1999). Novelty acquisition is associated with induction of hippocampal long-term depression. Proceedings of the National Academy of Sciences of the USA, 96, 8739-8744.
Manahan-Vaughan, D., Braunewell, K.-H., & Reymann, K. G. (1998). Subtype-specific involvement of metabotropic glutamate receptors in two forms of long-term potentiation in the dentate gyrus of freely moving rats. Neuroscience, 86, 709-721.
Manahan-Vaughan, D., Kulla, A., & Frey, J. U. (2000). Requirement of translation but not transcription for the maintenance of long-term depression in the CA1 region of freely moving rats. The Journal of Neuroscience, 20, 8572-8576.
Manahan-Vaughan, D., Reiser, M., Pin, J.-P., Wilsch, V., Bockaert, J., Reymann, K. G., & Riedel, G. (1996). Physiological and pharmacological profile oftrans-azetidine-2,4-dicarboxylic acid: Metabotropic glutamate receptor agonism and effects on long-term potentiation. Neuroscience, 72, 999-1008.
McNaughton, B. L., & Barnes, C. A. (1977). Physiological identification and analysis of dentate granule cell responses to stimulation of the medial and lateral perforant pathways in the rat. The Journal of Comparative Neurology, 175, 439-454.
Méndez-Couz, M., Becker, J. M., & Manahan-Vaughan, D. (2019). Functional compartmentalization of the contribution of hippocampal subfields to context-dependent extinction learning. Frontiers in Behavioral Neuroscience, 13, 256.
Mishkin, M., Ungerleider, L. G., & Macko, K. A. (1983). Object vision and spatial vision: Two cortical pathways. Trends in Neuroscience, 6, 414-417.
Montarolo, P. G., Goelet, P., Castellucci, V. F., Morgan, J., Kandel, E. R., & Schacher, S. (1986). A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science, 234, 1249-1254.
Montes-Rodríguez, C. J., Lapointe, V., Trivedi, V., Lu, Q., Demchuk, A. M., & McNaughton, B. L. (2013). Postnatal development of Homer1a in the rat hippocampus. Hippocampus, 23, 890-902.
Morgan, J. I., Cohen, D. R., Hempstead, J. L., & Curran, T. (1987). Mapping patterns of c-fos expression in the central nervous system after seizure. Science, 237, 192-197.
Naber, P. A., Lopes da Silva, F. H., & Witter, M. P. (2001). Reciprocal connections between the entorhinal cortex and hippocampal fields CA1 and the subiculum are in register with the projections from CA1 to the subiculum. Hippocampus, 11, 99-104.
Nakamura, N. H., Flasbeck, V., Maingret, N., Kitsukawa, T., & Sauvage, M. M. (2013). Proximodistal segregation of nonspatial information in CA3: Preferential recruitment of a proximal CA3-distal CA1 network in nonspatial recognition memory. The Journal of Neurocience, 33, 11506-11514.
Nguyen, P. V., & Kandel, E. R. (1996). A macromolecular synthesis-dependent late phase of long-term potentiation requiring cAMP in the medial perforant pathway of rat hippocampal slices. The Journal of Neuroscience, 16, 3189-3198.
Okada, D., Ozawa, F., & Inokuchi, K. (2009). Input-specific spine entry of soma-derived Vesl-1S protein conforms to synaptic tagging. Science, 324, 904-909.
Okuno, H., Akashi, K., Ishii, Y., Yagishita-Kyo, N., Suzuki, K., Nonaka, M., … Bito, H. (2012). Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3.1 with CaMKIIβ. Cell, 149, 886-898.
Peebles, C. L., Yoo, J., Thwin, M. T., Palop, J. J., Noebels, J. L., & Finkbeiner, S. (2010). Arc regulates spine morphology and maintains network stability in vivo. Proceedings of the National Academy of Sciences of the USA, 107, 18173-18178.
Plath, N., Ohana, O., Dammermann, B., Errington, M. L., Schmitz, D., Gross, C., … Kuhl, D. (2006). Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron, 52, 437-444.
Quirk, G. J. (2002). Memory for extinction of conditioned fear is long-lasting and persists following spontaneous recovery. Learning and Memory, 9, 402-407.
Reymann, K. G., & Frey, J. U. (2007). The late maintenance of hippocampal LTP: Requirements, phases, “synaptic tagging,” “late-associativity” and implications. Neuropharmacology, 52, 24-40.
Sajikumar, S., Navakkode, S., & Frey, J. U. (2007). Identification of compartment- and process-specific molecules required for "synaptic tagging" during long-term potentiation and long-term depression in hippocampal CA1. The Journal of Neuroscience, 27, 5068-5080.
Saunderson, E. A., Spiers, H., Mifsud, K. R., Gutierrez-Mecinas, M., Trollope, A. F., Shaikh, A., … Reul, J. M. H. M. (2016). Stress-induced gene expression and behavior are controlled by DNA methylation and methyl donor availability in the dentate gyrus. Proceedings of the National Academy of Sciences of the USA, 113, 4830-4835.
Sauvage, M. M., Nakamura, N. H., & Beer, Z. (2013). Mapping memory function in the medial temporal lobe with the immediate-early gene arc. Behavioural Brain Research, 254, 22-33.
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., … Cardona, A. (2012). Fiji: An open-source platform for biological-image analysis. Nature Methods, 9, 676-682.
Schwartz, J. H., Castellucci, V. F., & Kandel, E. R. (1971). Functioning of identified neurons and synapses in abdominal ganglion of Aplysia in absence of protein synthesis. Journal of Neurophysiology, 34, 939-953.
Steward, O. (1976). Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. The Journal of Comparative Neurology, 167, 285-314.
Steward, O., & Scoville, S. A. (1976). Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. The Journal of Comparative Neurology, 169, 347-370.
Straube, T., Korz, V., & Frey, J. U. (2003). Bidirectional modulation of long-term potentiation by novelty-exploration in rat dentate gyrus. Neuroscience Letters, 344, 5-8.
Suh, J., Rivest, A. J., Nakashiba, T., Tominaga, T., & Tonegawa, S. (2011). Entorhinal cortex layer III input to the hippocampus is crucial for temporal association memory. Science, 334, 1415-1420.
Tamamaki, N. (1997). Organization of the entorhinal projection to the rat dentate gyrus revealed by Dil anterograde labeling. Experimental Brain Research, 116, 250-258.
Tamamaki, N., & Nojyo, Y. (1995). Preservation of topography in the connections between the subiculum, field CA1, and the entorhinal cortex in rats. The Journal of Comparative Neurology, 353, 379-390.
Tang, S. H., Reis, G., Kang, H., Gingras, A.-C., Sonenberg, N., & Schuman, E. M. (2002). A rampamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proceeding of National Academy of Sciences of the USA, 99, 467-472.
Tully, T., Preat, T., Boynton, S. C., & Del Vecchio, M. (1994). Genetic dissection of consolidated memory in drosophila. Cell, 79, 35-47.
van Cauter, T., Camon, J., Alvernhe, A., Elduayen, C., Sargolini, F., & Save, E. (2013). Distinct roles of medial and lateral entorhinal cortex in spatial cognition. Cerebral Cortex, 23, 451-459.
van Groen, T., Kadish, I., & Wyss, J. M. (2002). Species differences in the projections from the entorhinal cortex to the hippocampus. Brain Research Bulletin, 57, 553-556.
Vazdarjanova, A., McNaughton, B. L., Barnes, C. A., Worley, P. F., & Guzowski, J. F. (2002). Experience-dependent coincident expression of the effector immediate-early genes Arc and Homer 1a in hippocampal and neocortical neuronal networks. The Journal of Neurocience, 22, 10067-10071.
Witter, M. P., & Amaral, D. G. (1991). Entorhinal cortex of the monkey: V. Projections to the dentate gyrus, hippocampus, and subicular complex. The Journal of Comparative Neurology, 307, 437-459.
Witter, M. P., Griffioen, A. W., Jorritsma-Byham, B., & Krijnen, J. L. M. (1988). Entorhinal projections to the hippocampal CA1 region in the rat: An underestimated pathway. Neuroscience Letters, 85, 193-198.
Witter, M. P., van Hoesen, G. W., & Amaral, D. G. (1989). Topographical organization of the entorhinal projection to the dentate gyrus of the monkey. The Journal of Neuroscience, 9, 216-228.
Worley, P. F., Bhat, R. V., Baraban, J. M., Erickson, C. A., McNaughton, B. L., & Barnes, C. A. (1993). Thresholds for synaptic activation of transcription factors in hippocampus: Correlation with long-term enhancement. The Journal of Neuroscience, 13, 4776-4786.
Wyss, J. M. (1981). An autoradiographic study of the efferent connections of the entorhinal cortex in the rat. The Journal of Comparative Neurology, 199, 495-512.
Yin, J. C. P., Wallach, J. S., Del Vecchio, M., Wilder, E. L., Zhou, H., Quinn, W. G., & Tully, T. (1994). Induction of a dominant negative CREB transgene specifically blocks long-term memory in drosophila. Cell, 79, 49-58.

Auteurs

Thu-Huong Hoang (TH)

Medical Faculty, Department of Neurophysiology, Ruhr University Bochum, Bochum, Germany.
International Graduate School of Neuroscience, Ruhr University Bochum, Bochum, Germany.

Juliane Böge (J)

Medical Faculty, Department of Neurophysiology, Ruhr University Bochum, Bochum, Germany.

Denise Manahan-Vaughan (D)

Medical Faculty, Department of Neurophysiology, Ruhr University Bochum, Bochum, Germany.

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