Abstract
The maturation of cortical inhibition provided by parvalbumin-containing basket cells derived from the medial ganglionic eminence (MGE) is a key event in starting the enhanced visual cortical plasticity during the critical period. Although it is generally assumed that a further increase in inhibition closes the critical period again, it was recently shown that embryonic interneurons derived from the MGE can induce an additional, artificial critical period when injected into the visual cortex of young mice. It has, however, remained open whether this effect was indeed specific for MGE-derived cells, and whether critical period-like plasticity could also be induced in fully adult animals. To clarify these issues, we injected explants from either the MGE or the caudal ganglionic eminence (CGE) into the visual cortices of fully adult mice, and performed monocular deprivation 33 days later for 4 days. Animals implanted with MGE cells, but not with CGE cells, showed marked ocular dominance plasticity. Immunohistochemistry confirmed that the injected cells from both sources migrated far in the host cortex, that most developed into neurons producing GABA, and that only cells from the MGE expressed parvalbumin. Thus, our results confirm that the plasticity-inducing effect of embryonic interneurons is specific for cells from the MGE, and is independent of the host animal’s age.
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References
Alvarez-Dolado M et al (2006) Cortical inhibition modified by embryonic neural precursors grafted into the postnatal brain. J Neurosci 26:7380–7389. doi:10.1523/JNEUROSCI.1540-06.2006
Atallah BV, Bruns W, Carandini M, Scanziani M (2012) Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli. Neuron 73:159–170
Beurdeley M et al (2012) Otx2 binding to perineuronal nets persistently regulates plasticity in the mature visual cortex. J Neurosci 32:9429–9437. doi:10.1523/JNEUROSCI.0394-12.2012
Blakemore C, Garey LJ, Vital-Durand F (1978) The physiological effects of monocular deprivation and their reversal in the monkey’s visual cortex. J Physiol 283:223–262
Cang J, Kalatsky VA, Löwel S, Stryker MP (2005) Optical imaging of the intrinsic signal as a measure of cortical plasticity in the mouse. Vis Neurosci 22:685–691. doi:10.1017/S0952523805225178
Cellerino A, Siciliano R, Domenici L, Maffei L (1992) Parvalbumin immunoreactivity: a reliable marker for the effects of monocular deprivation in the rat visual cortex. Neuroscience 51:749–753
Davis MF, Figueroa Velez DX, Guevarra RP, Yang MC, Habeeb M, Carathedathu MC, Gandhi SP (2015) Inhibitory neuron transplantation into adult visual cortex creates a new critical period that rescues impaired vision. Neuron 86:1055–1066. doi:10.1016/j.neuron.2015.03.062
Daw NW, Fox K, Sato H, Czepita D (1992) Critical period for monocular deprivation in the cat visual cortex. J Neurophysiol 67:197–202
Fagiolini M, Hensch TK (2000) Inhibitory threshold for critical-period activation in primary visual cortex. Nature 404:183–186. doi:10.1038/35004582
Fagiolini M, Pizzorusso T, Berardi N, Domenici L, Maffei L (1994) Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vis Res 34:709–720
Fu Y et al (2014) A cortical circuit for gain control by behavioral state. Cell 156:1139–1152. doi:10.1016/j.cell.2014.01.050
Fu Y, Kaneko M, Tang Y, Alvarez-Buylla A, Stryker MP (2015) A cortical disinhibitory circuit for enhancing adult plasticity. eLife 4:e05558. doi:10.7554/eLife.05558
Gelman DM, Martini FJ, Nobrega-Pereira S, Pierani A, Kessaris N, Marin O (2009) The embryonic preoptic area is a novel source of cortical GABAergic interneurons. J Neurosci 29:9380–9389. doi:10.1523/JNEUROSCI.0604-09.2009
Gordon JA, Stryker MP (1996) Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J Neurosci 16:3274–3286
Hanover JL, Huang ZJ, Tonegawa S, Stryker MP (1999) Brain-derived neurotrophic factor overexpression induces precocious critical period in mouse visual cortex. J Neurosci 19:RC40
Harauzov A et al (2010) Reducing intracortical inhibition in the adult visual cortex promotes ocular dominance plasticity. J Neurosci 30:361–371. doi:10.1523/JNEUROSCI.2233-09.2010
Hensch TK, Fagiolini M, Mataga N, Stryker MP, Baekkeskov S, Kash SF (1998) Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282:1504–1508
Huang ZJ et al (1999) BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98:739–755 (pii:S0092-8674(00)81509-3)
Hunt RF, Girskis KM, Rubenstein JL, Alvarez-Buylla A, Baraban SC (2013) GABA progenitors grafted into the adult epileptic brain control seizures and abnormal behavior. Nat Neurosci 16:692–697. doi:10.1038/nn.3392
Inan M, Welagen J, Anderson SA (2012) Spatial and temporal bias in the mitotic origins of somatostatin- and parvalbumin-expressing interneuron subgroups and the chandelier subtype in the medial ganglionic eminence. Cereb Cortex 22:820–827. doi:10.1093/cercor/bhr148
Kalatsky VA, Stryker MP (2003) New paradigm for optical imaging: temporally encoded maps of intrinsic signal. Neuron 38:529–545 (pii:S0896627303002861)
Kaneko M, Stryker MP (2014) Sensory experience during locomotion promotes recovery of function in adult visual cortex. eLife 3:e02798. doi:10.7554/eLife.02798
Lee SH et al (2012) Activation of specific interneurons improves V1 feature selectivity and visual perception. Nature 488:379–383. doi:10.1038/nature11312
Lehmann K, Isstas M, Teichert M, Knölker V, Bolz J (2014) Cells from the medial, but not the caudal ganglionic eminence induce ocular dominance plasticity in adult mice. In: FENS forum 2015, Milan, p 2817
Lehmann K, Löwel S (2008) Age-dependent ocular dominance plasticity in adult mice. PLoS One 3:e3120. doi:10.1371/journal.pone.0003120
Lehmann K, Schmidt KF, Löwel S (2012) Vision and visual plasticity in ageing mice. Restor Neurol Neurosci 30:161–178. doi:10.3233/RNN-2012-110192
Marin O (2012) Interneuron dysfunction in psychiatric disorders. Nat Rev Neurosci 13:107–120. doi:10.1038/nrn3155
Martinez-Cerdeno V et al (2010) Embryonic MGE precursor cells grafted into adult rat striatum integrate and ameliorate motor symptoms in 6-OHDA-lesioned rats. Cell Stem Cell 6:238–250. doi:10.1016/j.stem.2010.01.004
Maya Vetencourt JF et al (2008) The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science 320:385–388. doi:10.1126/science.1150516
Maya Vetencourt JF, Tiraboschi E, Spolidoro M, Castren E, Maffei L (2011) Serotonin triggers a transient epigenetic mechanism that reinstates adult visual cortex plasticity in rats. Eur J Neurosci 33:49–57. doi:10.1111/j.1460-9568.2010.07488.x
Maya-Vetencourt JF et al (2012) Experience-dependent expression of NPAS4 regulates plasticity in adult visual cortex. J Physiol 590:4777–4787. doi:10.1113/jphysiol.2012.234237
Miyoshi G et al (2010) Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci 30:1582–1594. doi:10.1523/JNEUROSCI.4515-09.2010
Morishita H, Miwa JM, Heintz N, Hensch TK (2010) Lynx1, a cholinergic brake, limits plasticity in adult visual cortex. Science 330:1238–1240. doi:10.1126/science.1195320
Rudolph J, Gerstmann K, Zimmer G, Steinecke A, Doding A, Bolz J (2014) A dual role of EphB1/ephrin-B3 reverse signaling on migrating striatal and cortical neurons originating in the preoptic area: should I stay or go away? Front Cell Neurosci 8:185. doi:10.3389/fncel.2014.00185
Southwell DG, Froemke RC, Alvarez-Buylla A, Stryker MP, Gandhi SP (2010) Cortical plasticity induced by inhibitory neuron transplantation. Science 327:1145–1148. doi:10.1126/science.1183962
Southwell DG et al (2012) Intrinsically determined cell death of developing cortical interneurons. Nature 491:109–113. doi:10.1038/nature11523
Southwell DG, Nicholas CR, Basbaum AI, Stryker MP, Kriegstein AR, Rubenstein JL, Alvarez-Buylla A (2014) Interneurons from embryonic development to cell-based therapy. Science 344:1240622. doi:10.1126/science.1240622
Spiegel I et al (2014) Npas4 regulates excitatory-inhibitory balance within neural circuits through cell-type-specific gene programs. Cell 157:1216–1229. doi:10.1016/j.cell.2014.03.058
Sugiyama S, Di Nardo AA, Aizawa S, Matsuo I, Volovitch M, Prochiantz A, Hensch TK (2008) Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity. Cell 134:508–520. doi:10.1016/j.cell.2008.05.054
Tanaka DH, Toriumi K, Kubo K, Nabeshima T, Nakajima K (2011) GABAergic precursor transplantation into the prefrontal cortex prevents phencyclidine-induced cognitive deficits. J Neurosci 31:14116–14125. doi:10.1523/JNEUROSCI.2786-11.2011
Tang Y, Stryker MP, Alvarez-Buylla A, Espinosa JS (2014) Cortical plasticity induced by transplantation of embryonic somatostatin or parvalbumin interneurons. Proc Natl Acad Sci USA 111:18339–18344. doi:10.1073/pnas.1421844112
Tong LM et al (2014) Inhibitory interneuron progenitor transplantation restores normal learning and memory in ApoE4 knock-in mice without or with Abeta accumulation. J Neurosci 34:9506–9515. doi:10.1523/JNEUROSCI.0693-14.2014
Wichterle H, Garcia-Verdugo JM, Herrera DG, Alvarez-Buylla A (1999) Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat Neurosci 2:461–466. doi:10.1038/8131
Wilson NR, Runyan CA, Wang FL, Sur M (2012) Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 488:343–348. doi:10.1038/nature11347
Wonders CP, Taylor L, Welagen J, Mbata IC, Xiang JZ, Anderson SA (2008) A spatial bias for the origins of interneuron subgroups within the medial ganglionic eminence. Dev Biol 314:127–136. doi:10.1016/j.ydbio.2007.11.018
Xu Q, Cobos I, De La Cruz E, Rubenstein JL, Anderson SA (2004) Origins of cortical interneuron subtypes. J Neurosci 24:2612–2622. doi:10.1523/JNEUROSCI.5667-03.2004
Yazaki-Sugiyama Y, Kang S, Cateau H, Fukai T, Hensch TK (2009) Bidirectional plasticity in fast-spiking GABA circuits by visual experience. Nature 462:218–221. doi:10.1038/nature08485
Yeritsyan N, Lehmann K, Puk O, Graw J, Lowel S (2012) Visual capabilities and cortical maps in BALB/c mice. Eur J Neurosci 36:2801–2811. doi:10.1111/j.1460-9568.2012.08195.x
Zimmer G, Rudolph J, Landmann J, Gerstmann K, Steinecke A, Gampe C, Bolz J (2011) Bidirectional ephrinB3/EphA4 signaling mediates the segregation of medial ganglionic eminence- and preoptic area-derived interneurons in the deep and superficial migratory stream. J Neurosci 31:18364–18380. doi:10.1523/JNEUROSCI.4690-11.2011
Acknowledgments
We are grateful to Vanessa Knölker for help with data analysis, Elisabeth Meier for excellent technical assistance, and to Sandra Clemens for animal care. We further wish to thank Prof. Christian Hübner and Dr. Lutz Liebmann (Institute for Human Genetics, Jena) for their willingness to cooperate, and Dr. Annika Döding for proof-reading the manuscript.
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J. Bolz and K. Lehmann contributed equally.
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Isstas, M., Teichert, M., Bolz, J. et al. Embryonic interneurons from the medial, but not the caudal ganglionic eminence trigger ocular dominance plasticity in adult mice. Brain Struct Funct 222, 539–547 (2017). https://doi.org/10.1007/s00429-016-1232-y
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DOI: https://doi.org/10.1007/s00429-016-1232-y