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  • Perspective
  • Published:

Developmental timing and critical windows for the treatment of psychiatric disorders

Abstract

There is a growing understanding that pathological genetic variation and environmental insults during sensitive periods in brain development have long-term consequences on brain function, which range from learning disabilities to complex psychiatric disorders such as schizophrenia. Furthermore, recent experiments in animal models suggest that therapeutic interventions during sensitive periods, typically before the onset of clear neurological and behavioral symptoms, might prevent or ameliorate the development of specific pathologies. These studies suggest that understanding the dynamic nature of the pathophysiological mechanisms underlying psychiatric disorders is crucial for the development of effective therapies. In this Perspective, I explore the emerging concept of developmental windows in psychiatric disorders, their relevance for understanding disease progression and their potential for the design of new therapies. The limitations and caveats of early interventions in psychiatric disorders are also discussed in this context.

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Figure 1: Age of diagnosis for several neuropsychiatric disorders in relation to key processes in human neurodevelopment.
Figure 2: Brain regions and cell types affected in schizophrenia.
Figure 3: Milestones in the development of neural networks in the mouse neocortex.
Figure 4: Maturation of PV+ interneurons and critical-period plasticity.

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References

  1. Gore, F.M. et al. Global burden of disease in young people aged 10–24 years: a systematic analysis. Lancet 377, 2093–2102 (2011).

    Article  PubMed  Google Scholar 

  2. Lee, F.S. et al. Mental health. Adolescent mental health–opportunity and obligation. Science 346, 547–549 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. van Os, J. & Kapur, S. Schizophrenia. Lancet 374, 635–645 (2009).

    Article  CAS  PubMed  Google Scholar 

  4. Jeste, S.S. & Geschwind, D.H. Clinical trials for neurodevelopmental disorders: At a therapeutic frontier. Sci. Transl. Med. 8, 321fs1 (2016).

    Article  PubMed  CAS  Google Scholar 

  5. Johnson, M.B. et al. Functional and evolutionary insights into human brain development through global transcriptome analysis. Neuron 62, 494–509 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Jaffe, A.E. et al. Developmental regulation of human cortex transcription and its clinical relevance at single base resolution. Nat. Neurosci. 18, 154–161 (2015).

    Article  CAS  PubMed  Google Scholar 

  7. Hall, J., Trent, S., Thomas, K.L., O'Donovan, M.C. & Owen, M.J. Genetic risk for schizophrenia: convergence on synaptic pathways involved in plasticity. Biol. Psychiatry 77, 52–58 (2015).

    Article  CAS  PubMed  Google Scholar 

  8. Willsey, A.J. & State, M.W. Autism spectrum disorders: from genes to neurobiology. Curr. Opin. Neurobiol. 30, 92–99 (2015).

    Article  PubMed  CAS  Google Scholar 

  9. Sekar, A. et al. Schizophrenia risk from complex variation of complement component 4. Nature 530, 177–183 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Schmitt, A., Malchow, B., Hasan, A. & Falkai, P. The impact of environmental factors in severe psychiatric disorders. Front. Neurosci. 8, 19 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  11. Hübener, M. & Bonhoeffer, T. Neuronal plasticity: beyond the critical period. Cell 159, 727–737 (2014).

    Article  PubMed  CAS  Google Scholar 

  12. Kalia, A. et al. Development of pattern vision following early and extended blindness. Proc. Natl. Acad. Sci. USA 111, 2035–2039 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Millan, M.J. et al. Altering the course of schizophrenia: progress and perspectives. Nat. Rev. Drug Discov. 15, 485–515 (2016).

    Article  CAS  PubMed  Google Scholar 

  14. Veenstra-VanderWeele, J. & Warren, Z. Intervention in the context of development: pathways toward new treatments. Neuropsychopharmacology 40, 225–237 (2015).

    Article  PubMed  Google Scholar 

  15. Silbereis, J.C., Pochareddy, S., Zhu, Y., Li, M. & Sestan, N. The cellular and molecular landscapes of the developing human central nervous system. Neuron 89, 248–268 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Wiesel, T.N. & Hubel, D.H. Extent of recovery from the effects of visual deprivation in kittens. J. Neurophysiol. 28, 1060–1072 (1965).

    Article  CAS  PubMed  Google Scholar 

  17. Greenhill, S.D. et al. Neurodevelopment. Adult cortical plasticity depends on an early postnatal critical period. Science 349, 424–427 (2015).

    Article  CAS  PubMed  Google Scholar 

  18. Anderson, P.J. & Reidy, N. Assessing executive function in preschoolers. Neuropsychol. Rev. 22, 345–360 (2012).

    Article  PubMed  Google Scholar 

  19. Friedmann, N. & Rusou, D. Critical period for first language: the crucial role of language input during the first year of life. Curr. Opin. Neurobiol. 35, 27–34 (2015).

    Article  CAS  PubMed  Google Scholar 

  20. Rakic, P., Bourgeois, J.P. & Goldman-Rakic, P.S. Synaptic development of the cerebral cortex: implications for learning, memory, and mental illness. Prog. Brain Res. 102, 227–243 (1994).

    Article  CAS  PubMed  Google Scholar 

  21. Ebert, D.H. & Greenberg, M.E. Activity-dependent neuronal signalling and autism spectrum disorder. Nature 493, 327–337 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Penzes, P., Cahill, M.E., Jones, K.A., VanLeeuwen, J.E. & Woolfrey, K.M. Dendritic spine pathology in neuropsychiatric disorders. Nat. Neurosci. 14, 285–293 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Südhof, T.C. Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455, 903–911 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Marín, O. Interneuron dysfunction in psychiatric disorders. Nat. Rev. Neurosci. 13, 107–120 (2012).

    Article  PubMed  CAS  Google Scholar 

  25. Ben-Ari, Y. Excitatory actions of gaba during development: the nature of the nurture. Nat. Rev. Neurosci. 3, 728–739 (2002).

    Article  CAS  PubMed  Google Scholar 

  26. Ben-Ari, Y., Gaiarsa, J.L., Tyzio, R. & Khazipov, R. GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol. Rev. 87, 1215–1284 (2007).

    Article  CAS  PubMed  Google Scholar 

  27. Kirkby, L.A., Sack, G.S., Firl, A. & Feller, M.B. A role for correlated spontaneous activity in the assembly of neural circuits. Neuron 80, 1129–1144 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Uhlhaas, P.J., Roux, F., Rodriguez, E., Rotarska-Jagiela, A. & Singer, W. Neural synchrony and the development of cortical networks. Trends Cogn. Sci. 14, 72–80 (2010).

    Article  PubMed  Google Scholar 

  29. Tyzio, R. et al. Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery. Science 314, 1788–1792 (2006).

    Article  CAS  PubMed  Google Scholar 

  30. Mwaniki, M.K., Atieno, M., Lawn, J.E. & Newton, C.R. Long-term neurodevelopmental outcomes after intrauterine and neonatal insults: a systematic review. Lancet 379, 445–452 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  31. Ben-Ari, Y. Is birth a critical period in the pathogenesis of autism spectrum disorders? Nat. Rev. Neurosci. 16, 498–505 (2015).

    Article  CAS  PubMed  Google Scholar 

  32. Rochefort, N.L. et al. Sparsification of neuronal activity in the visual cortex at eye-opening. Proc. Natl. Acad. Sci. USA 106, 15049–15054 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Toyoizumi, T. et al. A theory of the transition to critical period plasticity: inhibition selectively suppresses spontaneous activity. Neuron 80, 51–63 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Nabel, E.M. & Morishita, H. Regulating critical period plasticity: insight from the visual system to fear circuitry for therapeutic interventions. Front. Psychiatry 4, 146 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Hubel, D.H. & Wiesel, T.N. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. (Lond.) 206, 419–436 (1970).

    Article  CAS  Google Scholar 

  36. Wang, B.S., Sarnaik, R. & Cang, J. Critical period plasticity matches binocular orientation preference in the visual cortex. Neuron 65, 246–256 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Hensch, T.K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6, 877–888 (2005).

    Article  CAS  PubMed  Google Scholar 

  38. Hu, H., Gan, J. & Jonas, P. Interneurons. Fast-spiking, parvalbumin+ GABAergic interneurons: from cellular design to microcircuit function. Science 345, 1255263 (2014).

    Article  PubMed  CAS  Google Scholar 

  39. Sigurdsson, T. & Duvarci, S. Hippocampal-prefrontal interactions in cognition, behavior and psychiatric disease. Front. Syst. Neurosci. 9, 190 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Leucht, S. et al. Second-generation versus first-generation antipsychotic drugs for schizophrenia: a meta-analysis. Lancet 373, 31–41 (2009).

    Article  CAS  PubMed  Google Scholar 

  41. Green, M.F. What are the functional consequences of neurocognitive deficits in schizophrenia? Am. J. Psychiatry 153, 321–330 (1996).

    Article  CAS  PubMed  Google Scholar 

  42. Weinberger, D.R. Implications of normal brain development for the pathogenesis of schizophrenia. Arch. Gen. Psychiatry 44, 660–669 (1987).

    Article  CAS  PubMed  Google Scholar 

  43. Rapoport, J.L., Giedd, J.N. & Gogtay, N. Neurodevelopmental model of schizophrenia: update 2012. Mol. Psychiatry 17, 1228–1238 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Insel, T.R. Rethinking schizophrenia. Nature 468, 187–193 (2010).

    Article  CAS  PubMed  Google Scholar 

  45. Wyatt, R.J. Neuroleptics and the natural course of schizophrenia. Schizophr. Bull. 17, 325–351 (1991).

    Article  CAS  PubMed  Google Scholar 

  46. Robinson, D. et al. Predictors of relapse following response from a first episode of schizophrenia or schizoaffective disorder. Arch. Gen. Psychiatry 56, 241–247 (1999).

    Article  CAS  PubMed  Google Scholar 

  47. Howes, O.D. et al. The nature of dopamine dysfunction in schizophrenia and what this means for treatment. Arch. Gen. Psychiatry 69, 776–786 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Honea, R., Crow, T.J., Passingham, D. & Mackay, C.E. Regional deficits in brain volume in schizophrenia: a meta-analysis of voxel-based morphometry studies. Am. J. Psychiatry 162, 2233–2245 (2005).

    Article  PubMed  Google Scholar 

  49. Lewis, D.A., Curley, A.A., Glausier, J.R. & Volk, D.W. Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia. Trends Neurosci. 35, 57–67 (2012).

    Article  CAS  PubMed  Google Scholar 

  50. Lewis, D.A., Hashimoto, T. & Volk, D.W. Cortical inhibitory neurons and schizophrenia. Nat. Rev. Neurosci. 6, 312–324 (2005).

    Article  CAS  PubMed  Google Scholar 

  51. Fusar-Poli, P. et al. Predicting psychosis: meta-analysis of transition outcomes in individuals at high clinical risk. Arch. Gen. Psychiatry 69, 220–229 (2012).

    Article  PubMed  Google Scholar 

  52. Howes, O. et al. Progressive increase in striatal dopamine synthesis capacity as patients develop psychosis: a PET study. Mol. Psychiatry 16, 885–886 (2011).

    Article  CAS  PubMed  Google Scholar 

  53. Fusar-Poli, P. et al. Progressive brain changes in schizophrenia related to antipsychotic treatment? A meta-analysis of longitudinal MRI studies. Neurosci. Biobehav. Rev. 37, 1680–1691 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Davidson, M. et al. Behavioral and intellectual markers for schizophrenia in apparently healthy male adolescents. Am. J. Psychiatry 156, 1328–1335 (1999).

    CAS  PubMed  Google Scholar 

  55. Lipska, B.K., Jaskiw, G.E. & Weinberger, D.R. Postpubertal emergence of hyperresponsiveness to stress and to amphetamine after neonatal excitotoxic hippocampal damage: a potential animal model of schizophrenia. Neuropsychopharmacology 9, 67–75 (1993).

    Article  CAS  PubMed  Google Scholar 

  56. Modinos, G., Allen, P., Grace, A.A. & McGuire, P. Translating the MAM model of psychosis to humans. Trends Neurosci. 38, 129–138 (2015).

    Article  CAS  PubMed  Google Scholar 

  57. Jones, C.A., Watson, D.J. & Fone, K.C. Animal models of schizophrenia. Br. J. Pharmacol. 164, 1162–1194 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Yoon, K.J. et al. Modeling a genetic risk for schizophrenia in iPSCs and mice reveals neural stem cell deficits associated with adherens junctions and polarity. Cell Stem Cell 15, 79–91 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Shcheglovitov, A. et al. SHANK3 and IGF1 restore synaptic deficits in neurons from 22q13 deletion syndrome patients. Nature 503, 267–271 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Brennand, K.J. et al. Modelling schizophrenia using human induced pluripotent stem cells. Nature 473, 221–225 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Kaiser, T. & Feng, G. Modeling psychiatric disorders for developing effective treatments. Nat. Med. 21, 979–988 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Richtand, N.M. et al. Risperidone pretreatment prevents elevated locomotor activity following neonatal hippocampal lesions. Neuropsychopharmacology 31, 77–89 (2006).

    Article  CAS  PubMed  Google Scholar 

  63. McGlashan, T.H. et al. Randomized, double-blind trial of olanzapine versus placebo in patients prodromally symptomatic for psychosis. Am. J. Psychiatry 163, 790–799 (2006).

    Article  PubMed  Google Scholar 

  64. Kim, I.H. et al. Spine pruning drives antipsychotic-sensitive locomotion via circuit control of striatal dopamine. Nat. Neurosci. 18, 883–891 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Kraguljac, N.V., White, D.M., Reid, M.A. & Lahti, A.C. Increased hippocampal glutamate and volumetric deficits in unmedicated patients with schizophrenia. JAMA Psychiatry 70, 1294–1302 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Schobel, S.A. et al. Imaging patients with psychosis and a mouse model establishes a spreading pattern of hippocampal dysfunction and implicates glutamate as a driver. Neuron 78, 81–93 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Brugger, S., Davis, J.M., Leucht, S. & Stone, J.M. Proton magnetic resonance spectroscopy and illness stage in schizophrenia--a systematic review and meta-analysis. Biol. Psychiatry 69, 495–503 (2011).

    Article  PubMed  Google Scholar 

  68. Del Pino, I. et al. Erbb4 deletion from fast-spiking interneurons causes schizophrenia-like phenotypes. Neuron 79, 1152–1168 (2013).

    Article  CAS  PubMed  Google Scholar 

  69. Andreou, C. et al. Increased resting-state gamma-band connectivity in first-episode schizophrenia. Schizophr. Bull. 41, 930–939 (2015).

    Article  PubMed  Google Scholar 

  70. Sun, L. et al. Evidence for dysregulated high-frequency oscillations during sensory processing in medication-naïve, first episode schizophrenia. Schizophr. Res. 150, 519–525 (2013).

    Article  PubMed  Google Scholar 

  71. Du, Y. & Grace, A.A. Peripubertal diazepam administration prevents the emergence of dopamine system hyperresponsivity in the MAM developmental disruption model of schizophrenia. Neuropsychopharmacology 38, 1881–1888 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Rudolph, U. & Knoflach, F. Beyond classical benzodiazepines: novel therapeutic potential of GABAA receptor subtypes. Nat. Rev. Drug Discov. 10, 685–697 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Schizophrenia Working Group of the Psychiatric Genomics Consortium. Biological insights from 108 schizophrenia-associated genetic loci. Nature 511, 421–427 (2014).

  74. Karayiorgou, M. et al. Schizophrenia susceptibility associated with interstitial deletions of chromosome 22q11. Proc. Natl. Acad. Sci. USA 92, 7612–7616 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Karayiorgou, M., Simon, T.J. & Gogos, J.A. 22q11.2 microdeletions: linking DNA structural variation to brain dysfunction and schizophrenia. Nat. Rev. Neurosci. 11, 402–416 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Green, T. et al. Psychiatric disorders and intellectual functioning throughout development in velocardiofacial (22q11.2 deletion) syndrome. J. Am. Acad. Child Adolesc. Psychiatry 48, 1060–1068 (2009).

    Article  PubMed  Google Scholar 

  77. Sigurdsson, T., Stark, K.L., Karayiorgou, M., Gogos, J.A. & Gordon, J.A. Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia. Nature 464, 763–767 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Mukai, J. et al. Molecular substrates of altered axonal growth and brain connectivity in a mouse model of schizophrenia. Neuron 86, 680–695 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Tamura, M., Mukai, J., Gordon, J.A. & Gogos, J.A. Developmental inhibition of Gsk3 rescues behavioral and neurophysiological deficits in a mouse model of schizophrenia predisposition. Neuron 89, 1100–1109 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Do, K.Q. et al. Schizophrenia: glutathione deficit in cerebrospinal fluid and prefrontal cortex in vivo. Eur. J. Neurosci. 12, 3721–3728 (2000).

    Article  CAS  PubMed  Google Scholar 

  81. Steullet, P. et al. Redox dysregulation affects the ventral but not dorsal hippocampus: impairment of parvalbumin neurons, gamma oscillations, and related behaviors. J. Neurosci. 30, 2547–2558 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Cabungcal, J.H. et al. Juvenile antioxidant treatment prevents adult deficits in a developmental model of schizophrenia. Neuron 83, 1073–1084 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Behrens, M.M. et al. Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase. Science 318, 1645–1647 (2007).

    Article  CAS  PubMed  Google Scholar 

  84. Morishita, H., Cabungcal, J.H., Chen, Y., Do, K.Q. & Hensch, T.K. Prolonged period of cortical plasticity upon redox dysregulation in fast-spiking interneurons. Biol. Psychiatry 78, 396–402 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Farokhnia, M. et al. N-acetylcysteine as an adjunct to risperidone for treatment of negative symptoms in patients with chronic schizophrenia: a randomized, double-blind, placebo-controlled study. Clin. Neuropharmacol. 36, 185–192 (2013).

    Article  CAS  PubMed  Google Scholar 

  86. Do, K.Q., Cabungcal, J.H., Frank, A., Steullet, P. & Cuenod, M. Redox dysregulation, neurodevelopment, and schizophrenia. Curr. Opin. Neurobiol. 19, 220–230 (2009).

    Article  CAS  PubMed  Google Scholar 

  87. Koseki, T. et al. Exposure to enriched environments during adolescence prevents abnormal behaviours associated with histone deacetylation in phencyclidine-treated mice. Int. J. Neuropsychopharmacol. 15, 1489–1501 (2012).

    Article  CAS  PubMed  Google Scholar 

  88. Lee, H. et al. Early cognitive experience prevents adult deficits in a neurodevelopmental schizophrenia model. Neuron 75, 714–724 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Hagerman, R.J. et al. Advances in the treatment of fragile X syndrome. Pediatrics 123, 378–390 (2009).

    Article  PubMed  Google Scholar 

  90. Penagarikano, O., Mulle, J.G. & Warren, S.T. The pathophysiology of fragile X syndrome. Annu. Rev. Genomics Hum. Genet. 8, 109–129 (2007).

    Article  CAS  PubMed  Google Scholar 

  91. Santoro, M.R., Bray, S.M. & Warren, S.T. Molecular mechanisms of fragile X syndrome: a twenty-year perspective. Annu. Rev. Pathol. 7, 219–245 (2012).

    Article  CAS  PubMed  Google Scholar 

  92. Bear, M.F., Huber, K.M. & Warren, S.T. The mGluR theory of fragile X mental retardation. Trends Neurosci. 27, 370–377 (2004).

    Article  CAS  PubMed  Google Scholar 

  93. Garber, K.B., Visootsak, J. & Warren, S.T. Fragile X syndrome. Eur. J. Hum. Genet. 16, 666–672 (2008).

    Article  CAS  PubMed  Google Scholar 

  94. Bureau, I., Shepherd, G.M. & Svoboda, K. Circuit and plasticity defects in the developing somatosensory cortex of FMR1 knock-out mice. J. Neurosci. 28, 5178–5188 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Cruz-Martín, A., Crespo, M. & Portera-Cailliau, C. Delayed stabilization of dendritic spines in fragile X mice. J. Neurosci. 30, 7793–7803 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. Galvez, R. & Greenough, W.T. Sequence of abnormal dendritic spine development in primary somatosensory cortex of a mouse model of the fragile X mental retardation syndrome. Am. J. Med. Genet. A. 135, 155–160 (2005).

    Article  PubMed  Google Scholar 

  97. Harlow, E.G. et al. Critical period plasticity is disrupted in the barrel cortex of FMR1 knockout mice. Neuron 65, 385–398 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Nimchinsky, E.A., Oberlander, A.M. & Svoboda, K. Abnormal development of dendritic spines in FMR1 knock-out mice. J. Neurosci. 21, 5139–5146 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Dölen, G. et al. Correction of fragile X syndrome in mice. Neuron 56, 955–962 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. Kim, H., Gibboni, R., Kirkhart, C. & Bao, S. Impaired critical period plasticity in primary auditory cortex of fragile X model mice. J. Neurosci. 33, 15686–15692 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Till, S.M. et al. Altered maturation of the primary somatosensory cortex in a mouse model of fragile X syndrome. Hum. Mol. Genet. 21, 2143–2156 (2012).

    Article  CAS  PubMed  Google Scholar 

  102. Berry-Kravis, E. et al. Seizures in fragile X syndrome: characteristics and comorbid diagnoses. Am. J. Intellect. Dev. Disabil. 115, 461–472 (2010).

    Article  PubMed  Google Scholar 

  103. Musumeci, S.A. et al. Audiogenic seizures susceptibility in transgenic mice with fragile X syndrome. Epilepsia 41, 19–23 (2000).

    Article  CAS  PubMed  Google Scholar 

  104. Gonçalves, J.T., Anstey, J.E., Golshani, P. & Portera-Cailliau, C. Circuit level defects in the developing neocortex of Fragile X mice. Nat. Neurosci. 16, 903–909 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  105. Gibson, J.R., Bartley, A.F., Hays, S.A. & Huber, K.M. Imbalance of neocortical excitation and inhibition and altered UP states reflect network hyperexcitability in the mouse model of fragile X syndrome. J. Neurophysiol. 100, 2615–2626 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  106. Sourdet, V., Russier, M., Daoudal, G., Ankri, N. & Debanne, D. Long-term enhancement of neuronal excitability and temporal fidelity mediated by metabotropic glutamate receptor subtype 5. J. Neurosci. 23, 10238–10248 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Braat, S. & Kooy, R.F. The GABAA receptor as a therapeutic target for neurodevelopmental disorders. Neuron 86, 1119–1130 (2015).

    Article  CAS  PubMed  Google Scholar 

  108. He, Q., Nomura, T., Xu, J. & Contractor, A. The developmental switch in GABA polarity is delayed in fragile X mice. J. Neurosci. 34, 446–450 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Tyzio, R. et al. Oxytocin-mediated GABA inhibition during delivery attenuates autism pathogenesis in rodent offspring. Science 343, 675–679 (2014).

    Article  CAS  PubMed  Google Scholar 

  110. de Vrij, F.M. et al. Rescue of behavioral phenotype and neuronal protrusion morphology in Fmr1 KO mice. Neurobiol. Dis. 31, 127–132 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Michalon, A. et al. Chronic pharmacological mGlu5 inhibition corrects fragile X in adult mice. Neuron 74, 49–56 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Su, T. et al. Early continuous inhibition of group 1 mGlu signaling partially rescues dendritic spine abnormalities in the Fmr1 knockout mouse model for fragile X syndrome. Psychopharmacology (Berl.) 215, 291–300 (2011).

    Article  CAS  Google Scholar 

  113. Yan, Q.J., Rammal, M., Tranfaglia, M. & Bauchwitz, R.P. Suppression of two major Fragile X syndrome mouse model phenotypes by the mGluR5 antagonist MPEP. Neuropharmacology 49, 1053–1066 (2005).

    Article  CAS  PubMed  Google Scholar 

  114. Berry-Kravis, E. et al. Mavoglurant in fragile X syndrome: Results of two randomized, double-blind, placebo-controlled trials. Sci. Transl. Med. 8, 321ra5 (2016).

    Article  PubMed  CAS  Google Scholar 

  115. Scharf, S.H., Jaeschke, G., Wettstein, J.G. & Lindemann, L. Metabotropic glutamate receptor 5 as drug target for Fragile X syndrome. Curr. Opin. Pharmacol. 20, 124–134 (2015).

    Article  CAS  PubMed  Google Scholar 

  116. Berry-Kravis, E.M. et al. Effects of STX209 (arbaclofen) on neurobehavioral function in children and adults with fragile X syndrome: a randomized, controlled, phase 2 trial. Sci. Transl. Med. 4, 152ra127 (2012).

    Article  PubMed  CAS  Google Scholar 

  117. Lemonnier, E. et al. A randomised controlled trial of bumetanide in the treatment of autism in children. Transl. Psychiatry 2, e202 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Hadjikhani, N. et al. Improving emotional face perception in autism with diuretic bumetanide: a proof-of-concept behavioral and functional brain imaging pilot study. Autism 19, 149–157 (2015).

    Article  PubMed  Google Scholar 

  119. Marguet, S.L. et al. Treatment during a vulnerable developmental period rescues a genetic epilepsy. Nat. Med. 21, 1436–1444 (2015).

    Article  CAS  PubMed  Google Scholar 

  120. Chahrour, M. & Zoghbi, H.Y. The story of Rett syndrome: from clinic to neurobiology. Neuron 56, 422–437 (2007).

    Article  CAS  PubMed  Google Scholar 

  121. Hagberg, B. Clinical manifestations and stages of Rett syndrome. Ment. Retard. Dev. Disabil. Res. Rev. 8, 61–65 (2002).

    Article  PubMed  Google Scholar 

  122. Ausió, J., Martínez de Paz, A. & Esteller, M. MeCP2: the long trip from a chromatin protein to neurological disorders. Trends Mol. Med. 20, 487–498 (2014).

    Article  PubMed  CAS  Google Scholar 

  123. Katz, D.M. et al. Rett syndrome: crossing the threshold to clinical translation. Trends Neurosci. 39, 100–113 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Lombardi, L.M., Baker, S.A. & Zoghbi, H.Y. MECP2 disorders: from the clinic to mice and back. J. Clin. Invest. 125, 2914–2923 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  125. Durand, S. et al. NMDA receptor regulation prevents regression of visual cortical function in the absence of Mecp2. Neuron 76, 1078–1090 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Krishnan, K. et al. MeCP2 regulates the timing of critical period plasticity that shapes functional connectivity in primary visual cortex. Proc. Natl. Acad. Sci. USA 112, E4782–E4791 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Mierau, S.B., Patrizi, A., Hensch, T.K. & Fagiolini, M. Cell-specific regulation of N-methyl-D-aspartate receptor maturation by Mecp2 in cortical circuits. Biol. Psychiatry 79, 746–754 (2016).

    Article  CAS  PubMed  Google Scholar 

  128. Huang, Z.J. et al. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98, 739–755 (1999).

    Article  CAS  PubMed  Google Scholar 

  129. Dani, V.S. et al. Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett syndrome. Proc. Natl. Acad. Sci. USA 102, 12560–12565 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Moghaddam, B. & Krystal, J.H. Capturing the angel in “angel dust”: twenty years of translational neuroscience studies of NMDA receptor antagonists in animals and humans. Schizophr. Bull. 38, 942–949 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  131. Patrizi, A. et al. Chronic administration of the N-methyl-D-aspartate receptor antagonist ketamine improves Rett syndrome phenotype. Biol. Psychiatry 79, 755–764 (2016).

    Article  CAS  PubMed  Google Scholar 

  132. Kron, M. et al. Brain activity mapping in Mecp2 mutant mice reveals functional deficits in forebrain circuits, including key nodes in the default mode network, that are reversed with ketamine treatment. J. Neurosci. 32, 13860–13872 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Ehninger, D., Li, W., Fox, K., Stryker, M.P. & Silva, A.J. Reversing neurodevelopmental disorders in adults. Neuron 60, 950–960 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. McGraw, C.M., Samaco, R.C. & Zoghbi, H.Y. Adult neural function requires MeCP2. Science 333, 186 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Green, J. et al. Intervention for infants at risk of developing autism: a case series. J. Autism Dev. Disord. 43, 2502–2514 (2013).

    Article  PubMed  Google Scholar 

  136. Miklowitz, D.J. et al. Family-focused treatment for adolescents and young adults at high risk for psychosis: results of a randomized trial. J. Am. Acad. Child Adolesc. Psychiatry 53, 848–858 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  137. Larroque, B. et al. Neurodevelopmental disabilities and special care of 5-year-old children born before 33 weeks of gestation (the EPIPAGE study): a longitudinal cohort study. Lancet 371, 813–820 (2008).

    Article  PubMed  Google Scholar 

  138. Lin, A. et al. Outcomes of nontransitioned cases in a sample at ultra-high risk for psychosis. Am. J. Psychiatry 172, 249–258 (2015).

    Article  PubMed  Google Scholar 

  139. Bousman, C.A. et al. Effects of NRG1 and DAOA genetic variation on transition to psychosis in individuals at ultra-high risk for psychosis. Transl. Psychiatry 3, e251 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Corcoran, C.M. et al. HPA axis function and symptoms in adolescents at clinical high risk for schizophrenia. Schizophr. Res. 135, 170–174 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Perkins, D.O. et al. Towards a psychosis risk blood diagnostic for persons experiencing high-risk symptoms: preliminary results from the NAPLS project. Schizophr. Bull. 41, 419–428 (2015).

    Article  PubMed  Google Scholar 

  142. Egerton, A., Fusar-Poli, P. & Stone, J.M. Glutamate and psychosis risk. Curr. Pharm. Des. 18, 466–478 (2012).

    Article  CAS  PubMed  Google Scholar 

  143. Tognin, S. et al. Using structural neuroimaging to make quantitative predictions of symptom progression in individuals at ultra-high risk for psychosis. Front. Psychiatry 4, 187 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  144. Bodatsch, M., Brockhaus-Dumke, A., Klosterkötter, J. & Ruhrmann, S. Forecasting psychosis by event-related potentials-systematic review and specific meta-analysis. Biol. Psychiatry 77, 951–958 (2015).

    Article  PubMed  Google Scholar 

  145. Wolff, J.J. et al. Differences in white matter fiber tract development present from 6 to 24 months in infants with autism. Am. J. Psychiatry 169, 589–600 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  146. Jones, W. & Klin, A. Attention to eyes is present but in decline in 2-6-month-old infants later diagnosed with autism. Nature 504, 427–431 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Maayan, L. & Correll, C.U. Weight gain and metabolic risks associated with antipsychotic medications in children and adolescents. J. Child Adolesc. Psychopharmacol. 21, 517–535 (2011).

    Article  CAS  PubMed  Google Scholar 

  148. Ikonomidou, C. et al. Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 283, 70–74 (1999).

    Article  CAS  PubMed  Google Scholar 

  149. Bittigau, P. et al. Antiepileptic drugs and apoptotic neurodegeneration in the developing brain. Proc. Natl. Acad. Sci. USA 99, 15089–15094 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Brambrink, A.M. et al. Isoflurane-induced neuroapoptosis in the neonatal rhesus macaque brain. Anesthesiology 112, 834–841 (2010).

    Article  CAS  PubMed  Google Scholar 

  151. Schneider, M. et al. Psychiatric disorders from childhood to adulthood in 22q11.2 deletion syndrome: results from the International Consortium on Brain and Behavior in 22q11.2 Deletion Syndrome. Am. J. Psychiatry 171, 627–639 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  152. Kessler, R.C. et al. Age of onset of mental disorders: a review of recent literature. Curr. Opin. Psychiatry 20, 359–364 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  153. Kessler, R.C. et al. Lifetime prevalence and age-of-onset distributions of mental disorders in the World Health Organization's World Mental Health Survey Initiative. World Psychiatry 6, 168–176 (2007).

    PubMed  PubMed Central  Google Scholar 

  154. Pratt, J., Winchester, C., Dawson, N. & Morris, B. Advancing schizophrenia drug discovery: optimizing rodent models to bridge the translational gap. Nat. Rev. Drug Discov. 11, 560–579 (2012).

    Article  CAS  PubMed  Google Scholar 

  155. Dobbs, D. Schizophrenia: the making of a troubled mind. Nature 468, 154–156 (2010).

    Article  CAS  PubMed  Google Scholar 

  156. Le Magueresse, C. & Monyer, H. GABAergic interneurons shape the functional maturation of the cortex. Neuron 77, 388–405 (2013).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

I apologize for not citing all relevant references, owing to space limitations. I thank B. Rico and members of the Marín lab for valuable discussions and their critical reading of this manuscript. The European Research Council (ERC-2011-AdG 293683), Wellcome Trust (103714MA), Simons Foundation Autism Research Initiative (SFARI 239766OM) and De Spoelberch Foundation support work on this topic in my laboratory. O.M. is a Wellcome Trust Investigator.

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Marín, O. Developmental timing and critical windows for the treatment of psychiatric disorders. Nat Med 22, 1229–1238 (2016). https://doi.org/10.1038/nm.4225

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