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Lineage divergence of activity-driven transcription and evolution of cognitive ability

Abstract

Excitation–transcription coupling shapes network formation during brain development and controls neuronal survival, synaptic function and cognitive skills in the adult. New studies have uncovered differences in the transcriptional responses to synaptic activity between humans and mice. These differences are caused both by the emergence of lineage-specific activity-regulated genes and by the acquisition of signal-responsive DNA elements in gene regulatory regions that determine whether a gene can be transcriptionally induced by synaptic activity or alter the extent of its inducibility. Such evolutionary divergence may have contributed to lineage-related advancements in cognitive abilities.

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Figure 1: Linking evolutionary remodelling of promoter architectures to altered activity-dependent gene expression and cognitive abilities.

References

  1. Geschwind, D. H. & Rakic, P. Cortical evolution: judge the brain by its cover. Neuron 80, 633–647 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Izpisua Belmonte, J. C. et al. Brains, genes, and primates. Neuron 86, 617–631 (2015).

    PubMed  Google Scholar 

  3. Kaas, J. H. The evolution of brains from early mammals to humans. Wiley Interdiscip. Rev. Cogn. Sci. 4, 33–45 (2013).

    PubMed  Google Scholar 

  4. Necsulea, A. & Kaessmann, H. Evolutionary dynamics of coding and non-coding transcriptomes. Nat. Rev. Genet. 15, 734–748 (2014).

    CAS  PubMed  Google Scholar 

  5. King, M. C. & Wilson, A. C. Evolution at two levels in humans and chimpanzees. Science 188, 107–116 (1975).

    CAS  PubMed  Google Scholar 

  6. Konopka, G. et al. Human-specific transcriptional networks in the brain. Neuron 75, 601–617 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Nord, A. S., Pattabiraman, K., Visel, A. & Rubenstein, J. L. Genomic perspectives of transcriptional regulation in forebrain development. Neuron 85, 27–47 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Nord, A. S. et al. Rapid and pervasive changes in genome-wide enhancer usage during mammalian development. Cell 155, 1521–1531 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Shim, S., Kwan, K. Y., Li, M., Lefebvre, V. & Sestan, N. Cis-regulatory control of corticospinal system development and evolution. Nature 486, 74–79 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Kim, T. K. et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 465, 182–187 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Spiegel, I. et al. Npas4 regulates excitatory-inhibitory balance within neural circuits through cell-type-specific gene programs. Cell 157, 1216–1229 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Zhang, S. J. et al. Decoding NMDA receptor signaling: identification of genomic programs specifying neuronal survival and death. Neuron 53, 549–562 (2007).

    CAS  PubMed  Google Scholar 

  14. Zhang, S. J. et al. Nuclear calcium signaling controls expression of a large gene pool: identification of a gene program for acquired neuroprotection induced by synaptic activity. PLoS Genet. 5, e1000604 (2009).

    PubMed  PubMed Central  Google Scholar 

  15. Villar, D., Flicek, P. & Odom, D. T. Evolution of transcription factor binding in metazoans - mechanisms and functional implications. Nat. Rev. Genet. 15, 221–233 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Bading, H., Ginty, D. D. & Greenberg, M. E. Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 260, 181–186 (1993).

    CAS  PubMed  Google Scholar 

  17. Hong, E. J., McCord, A. E. & Greenberg, M. E. A biological function for the neuronal activity-dependent component of Bdnf transcription in the development of cortical inhibition. Neuron 60, 610–624 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Robertson, L. M. et al. Regulation of c-fos expression in transgenic mice requires multiple interdependent transcription control elements. Neuron 14, 241–252 (1995).

    CAS  PubMed  Google Scholar 

  19. Hardingham, G. E., Chawla, S., Johnson, C. M. & Bading, H. Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature 385, 260–265 (1997).

    CAS  PubMed  Google Scholar 

  20. Qiu, J. et al. Evidence for evolutionary divergence of activity-dependent gene expression in developing neurons. eLife 5, e20337 (2016).

    PubMed  PubMed Central  Google Scholar 

  21. Ataman, B. et al. Evolution of osteocrin as an activity-regulated factor in the primate brain. Nature 539, 242–247 (2016).

    PubMed  PubMed Central  Google Scholar 

  22. Pruunsild, P., Bengtson, C. P. & Bading, H. Networks of cultured iPSC-derived neurons reveal the human synaptic activity-regulated adaptive gene program. Cell Rep. 18, 122–135 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Bading, H. Nuclear calcium signalling in the regulation of brain function. Nat. Rev. Neurosci. 14, 593–608 (2013).

    CAS  PubMed  Google Scholar 

  24. Hardingham, G. E., Arnold, F. J. & Bading, H. Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat. Neurosci. 4, 261–267 (2001).

    CAS  PubMed  Google Scholar 

  25. Taylor, M. S. et al. Heterotachy in mammalian promoter evolution. PLoS Genet. 2, e30 (2006).

    PubMed  PubMed Central  Google Scholar 

  26. Kang, H. J. et al. Spatio-temporal transcriptome of the human brain. Nature 478, 483–489 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Moffatt, P. & Thomas, G. P. Osteocrin — beyond just another bone protein? Cell. Mol. Life Sci. 66, 1135–1139 (2009).

    CAS  PubMed  Google Scholar 

  28. Subbotina, E. et al. Musclin is an activity-stimulated myokine that enhances physical endurance. Proc. Natl Acad. Sci. USA 112, 16042–16047 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Dubuissez, M. et al. The Reelin receptors ApoER2 and VLDLR are direct target genes of HIC1 (Hypermethylated In Cancer 1). Biochem. Biophys. Res. Commun. 440, 424–430 (2013).

    CAS  PubMed  Google Scholar 

  30. Forster, E. et al. Emerging topics in Reelin function. Eur. J. Neurosci. 31, 1511–1518 (2010).

    PubMed  PubMed Central  Google Scholar 

  31. Miller, L. A. et al. CAMTA1 T polymorphism is associated with neuropsychological test performance in older adults with cardiovascular disease. Psychogeriatrics 11, 135–140 (2011).

    PubMed  Google Scholar 

  32. Thevenon, J. et al. Intragenic CAMTA1 rearrangements cause non-progressive congenital ataxia with or without intellectual disability. J. Med. Genet. 49, 400–408 (2012).

    CAS  PubMed  Google Scholar 

  33. Bas-Orth, C., Tan, Y. W., Oliveira, A. M., Bengtson, C. P. & Bading, H. The calmodulin-binding transcription activator CAMTA1 is required for long-term memory formation in mice. Learn. Mem. 23, 313–321 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Long, C. et al. Ataxia and Purkinje cell degeneration in mice lacking the CAMTA1 transcription factor. Proc. Natl Acad. Sci. USA 111, 11521–11526 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Finkler, A., Ashery-Padan, R. & Fromm, H. CAMTAs: calmodulin-binding transcription activators from plants to human. FEBS Lett. 581, 3893–3898 (2007).

    CAS  PubMed  Google Scholar 

  36. Liu, X. et al. Extension of cortical synaptic development distinguishes humans from chimpanzees and macaques. Genome Res. 22, 611–622 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Liu, X. et al. Disruption of an evolutionarily novel synaptic expression pattern in autism. PLoS Biol. 14, e1002558 (2016).

    PubMed  PubMed Central  Google Scholar 

  38. Luhmann, H. J., Fukuda, A. & Kilb, W. Control of cortical neuronal migration by glutamate and GABA. Front. Cell Neurosci. 9, 4 (2015).

    PubMed  PubMed Central  Google Scholar 

  39. Sun, T. & Hevner, R. F. Growth and folding of the mammalian cerebral cortex: from molecules to malformations. Nat. Rev. Neurosci. 15, 217–232 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Hemstedt, T. J., Bengtson, C. P., Ramirez, O., Oliveira, A. M. M. & Bading, H. Reciprocal interaction of dendrite geometry and nuclear calcium-VEGFD signaling gates memory consolidation and extinction. J. Neurosci. 37, 6946–6955 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Enard, W. The molecular basis of human brain evolution. Curr. Biol. 26, R1109–R1117 (2016).

    CAS  PubMed  Google Scholar 

  42. Li, Q. et al. Mice carrying a human GLUD2 gene recapitulate aspects of human transcriptome and metabolome development. Proc. Natl Acad. Sci. USA 113, 5358–5363 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Li, Q. et al. Changes in lipidome composition during brain development in humans, chimpanzees, and macaque monkeys. Mol. Biol. Evol. 34, 1155–1166 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Florio, M., Borrell, V. & Huttner, W. B. Human-specific genomic signatures of neocortical expansion. Curr. Opin. Neurobiol. 42, 33–44 (2017).

    CAS  PubMed  Google Scholar 

  45. Dehay, C., Kennedy, H. & Kosik, K. S. The outer subventricular zone and primate-specific cortical complexification. Neuron 85, 683–694 (2015).

    CAS  PubMed  Google Scholar 

  46. Rakic, P. Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 10, 724–735 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Fernandez, V., Llinares-Benadero, C. & Borrell, V. Cerebral cortex expansion and folding: what have we learned? EMBO J. 35, 1021–1044 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Bae, B. I., Jayaraman, D. & Walsh, C. A. Genetic changes shaping the human brain. Dev. Cell 32, 423–434 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Keeney, J. G. et al. DUF1220 protein domains drive proliferation in human neural stem cells and are associated with increased cortical volume in anthropoid primates. Brain Struct. Funct. 220, 3053–3060 (2015).

    CAS  PubMed  Google Scholar 

  50. Florio, M. et al. Human-specific gene ARHGAP11B promotes basal progenitor amplification and neocortex expansion. Science 347, 1465–1470 (2015).

    CAS  PubMed  Google Scholar 

  51. Ju, X. C. et al. The hominoid-specific gene TBC1D3 promotes generation of basal neural progenitors and induces cortical folding in mice. eLife 5, e18197 (2016).

    PubMed  PubMed Central  Google Scholar 

  52. Boyd, J. L. et al. Human-chimpanzee differences in a FZD8 enhancer alter cell-cycle dynamics in the developing neocortex. Curr. Biol. 25, 772–779 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Reilly, S. K. et al. Evolutionary genomics. Evolutionary changes in promoter and enhancer activity during human corticogenesis. Science 347, 1155–1159 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. de Juan Romero, C., Bruder, C., Tomasello, U., Sanz-Anquela, J. M. & Borrell, V. Discrete domains of gene expression in germinal layers distinguish the development of gyrencephaly. EMBO J. 34, 1859–1874 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Otani, T., Marchetto, M. C., Gage, F. H., Simons, B. D. & Livesey, F. J. 2D and 3D stem cell models of primate cortical development identify species-specific differences in progenitor behavior contributing to brain size. Cell Stem Cell 18, 467–480 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Mora-Bermúdez, F. et al. Differences and similarities between human and chimpanzee neural progenitors during cerebral cortex development. eLife 5, e18683 (2016).

    PubMed  PubMed Central  Google Scholar 

  57. Herculano-Houzel, S. Neuronal scaling rules for primate brains: the primate advantage. Prog. Brain Res. 195, 325–340 (2012).

    PubMed  Google Scholar 

  58. Hill, J. et al. Similar patterns of cortical expansion during human development and evolution. Proc. Natl Acad. Sci. USA 107, 13135–13140 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Gomez-Robles, A., Hopkins, W. D., Schapiro, S. J. & Sherwood, C. C. Relaxed genetic control of cortical organization in human brains compared with chimpanzees. Proc. Natl Acad. Sci. USA 112, 14799–14804 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Kwan, K. Y. et al. Species-dependent posttranscriptional regulation of NOS1 by FMRP in the developing cerebral cortex. Cell 149, 899–911 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Hage, S. R. & Nieder, A. Dual neural network model for the evolution of speech and language. Trends Neurosci. 39, 813–829 (2016).

    CAS  PubMed  Google Scholar 

  62. Greer, P. L. & Greenberg, M. E. From synapse to nucleus: calcium-dependent gene transcription in the control of synapse development and function. Neuron 59, 846–860 (2008).

    CAS  PubMed  Google Scholar 

  63. Hardingham, G. E. & Bading, H. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat. Rev. Neurosci. 11, 682–696 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Bading, H. Therapeutic targeting of the pathological triad of extrasynaptic NMDA receptor signaling in neurodegenerations. J. Exp. Med. 214, 569–578 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Hardingham, G. E., Fukunaga, Y. & Bading, H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat. Neurosci. 5, 405–414 (2002).

    CAS  PubMed  Google Scholar 

  66. Greenberg, M. E., Ziff, E. B. & Greene, L. A. Stimulation of neuronal acetylcholine receptors induces rapid gene transcription. Science 234, 80–83 (1986).

    CAS  PubMed  Google Scholar 

  67. Morgan, J. I. & Curran, T. Role of ion flux in the control of c-fos expression. Nature 322, 552–555 (1986).

    CAS  PubMed  Google Scholar 

  68. Worley, P. F. et al. Thresholds for synaptic activation of transcription factors in hippocampus: correlation with long-term enhancement. J. Neurosci. 13, 4776–4786 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Dolmetsch, R. E., Xu, K. & Lewis, R. S. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392, 933–936 (1998).

    CAS  PubMed  Google Scholar 

  70. Hagenston, A. M. & Bading, H. Calcium signaling in synapse-to-nucleus communication. Cold Spring Harb. Perspect. Biol. 3, a004564 (2011).

    PubMed  PubMed Central  Google Scholar 

  71. Bading, H. & Greenberg, M. E. Stimulation of protein tyrosine phosphorylation by NMDA receptor activation. Science 253, 912–914 (1991).

    CAS  PubMed  Google Scholar 

  72. Dieterich, D. C. et al. Caldendrin-Jacob: a protein liaison that couples NMDA receptor signalling to the nucleus. PLoS Biol. 6, e34 (2008).

    PubMed  PubMed Central  Google Scholar 

  73. Ch'ng, T. H. et al. Activity-dependent transport of the transcriptional coactivator CRTC1 from synapse to nucleus. Cell 150, 207–221 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Montarolo, P. G. et al. A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234, 1249–1254 (1986).

    CAS  PubMed  Google Scholar 

  75. Nguyen, P. V., Abel, T. & Kandel, E. R. Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265, 1104–1107 (1994).

    CAS  PubMed  Google Scholar 

  76. Tully, T., Preat, T., Boynton, S. C. & Del Vecchio, M. Genetic dissection of consolidated memory in Drosophila. Cell 79, 35–47 (1994).

    CAS  PubMed  Google Scholar 

  77. Chew, S. J., Mello, C., Nottebohm, F., Jarvis, E. & Vicario, D. S. Decrements in auditory responses to a repeated conspecific song are long-lasting and require two periods of protein synthesis in the songbird forebrain. Proc. Natl Acad. Sci. USA 92, 3406–3410 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Bell, K. F. & Hardingham, G. E. The influence of synaptic activity on neuronal health. Curr. Opin. Neurobiol. 21, 299–305 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Leslie, J. H. & Nedivi, E. Activity-regulated genes as mediators of neural circuit plasticity. Prog. Neurobiol. 94, 223–237 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Alberini, C. M. & Kandel, E. R. The regulation of transcription in memory consolidation. Cold Spring Harb. Perspect. Biol. 7, a021741 (2014).

    PubMed  Google Scholar 

  81. West, A. E. & Greenberg, M. E. Neuronal activity-regulated gene transcription in synapse development and cognitive function. Cold Spring Harb. Perspect. Biol. 3, a005744 (2011).

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Weislogel, J. M. et al. Requirement for nuclear calcium signaling in Drosophila long-term memory. Sci. Signal. 6, ra33 (2013).

    PubMed  Google Scholar 

  84. Mick, E. et al. Family-based genome-wide association scan of attention-deficit/hyperactivity disorder. J. Am. Acad. Child Adolesc. Psychiatry 49, 898–905.e3 (2010).

    PubMed  PubMed Central  Google Scholar 

  85. von Deimling, M. et al. Gene expression analysis in untreated absence epilepsy demonstrates an inconsistent pattern. Epilepsy Res. 132, 84–90 (2017).

    CAS  PubMed  Google Scholar 

  86. Huentelman, M. J. et al. Calmodulin-binding transcription activator 1 (CAMTA1) alleles predispose human episodic memory performance. Hum. Mol. Genet. 16, 1469–1477 (2007).

    CAS  PubMed  Google Scholar 

  87. Rajaraman, P. et al. Polymorphisms in apoptosis and cell cycle control genes and risk of brain tumors in adults. Cancer Epidemiol. Biomarkers Prev. 16, 1655–1661 (2007).

    CAS  PubMed  Google Scholar 

  88. Hellwig, D. et al. Dynamics of CENP-N kinetochore binding during the cell cycle. J. Cell Sci. 124, 3871–3883 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Park, B. et al. Association of Lbc Rho guanine nucleotide exchange factor with α-catenin-related protein, α-catulin/CTNNAL1, supports serum response factor activation. J. Biol. Chem. 277, 45361–45370 (2002).

    CAS  PubMed  Google Scholar 

  90. Kuwano, R. et al. Dynamin-binding protein gene on chromosome 10q is associated with late-onset Alzheimer's disease. Hum. Mol. Genet. 15, 2170–2182 (2006).

    CAS  PubMed  Google Scholar 

  91. Casoli, T. et al. Dynamin binding protein gene expression and memory performance in aged rats. Neurobiol. Aging 33, 618.e15–618.e19 (2012).

    CAS  Google Scholar 

  92. Patterson, K. I., Brummer, T., O'Brien, P. M. & Daly, R. J. Dual-specificity phosphatases: critical regulators with diverse cellular targets. Biochem. J. 418, 475–489 (2009).

    CAS  PubMed  Google Scholar 

  93. Wolvetang, E. J. et al. Overexpression of the chromosome 21 transcription factor Ets2 induces neuronal apoptosis. Neurobiol. Dis. 14, 349–356 (2003).

    CAS  PubMed  Google Scholar 

  94. Soong, B. W. et al. Exome sequencing identifies GNB4 mutations as a cause of dominant intermediate Charcot-Marie-Tooth disease. Am. J. Hum. Genet. 92, 422–430 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Arroyo-Carrera, I. et al. Deletion 1q43-44 in a patient with clinical diagnosis of Warburg-Micro syndrome. Am. J. Med. Genet. A 167A, 1243–1251 (2015).

    Google Scholar 

  96. Reitmair, A., Sachs, G., Im, W. B. & Wheeler, L. C6orf176: a novel possible regulator of cAMP-mediated gene expression. Physiol. Genom. 44, 152–161 (2012).

    CAS  Google Scholar 

  97. Katsuoka, F. et al. Small Maf compound mutants display central nervous system neuronal degeneration, aberrant transcription, and Bach protein mislocalization coincident with myoclonus and abnormal startle response. Mol. Cell. Biol. 23, 1163–1174 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Wharton, K. A. Jr., Zimmermann, G., Rousset, R. & Scott, M. P. Vertebrate proteins related to Drosophila Naked Cuticle bind Dishevelled and antagonize Wnt signaling. Dev. Biol. 234, 93–106 (2001).

    CAS  PubMed  Google Scholar 

  99. Seibt, J. et al. Expression at the imprinted Dlk1-Gtl2 locus is regulated by proneural genes in the developing telencephalon. PLoS ONE 7, e48675 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Lin, N. et al. An evolutionarily conserved long noncoding RNA TUNA controls pluripotency and neural lineage commitment. Mol. Cell 53, 1005–1019 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Yu, J. et al. Zinc-finger protein 331, a novel putative tumor suppressor, suppresses growth and invasiveness of gastric cancer. Oncogene 32, 307–317 (2013).

    CAS  PubMed  Google Scholar 

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H.B., G.E.H. and P.P. contributed equally to researching the data for the article and making substantial contributions to discussion of content. H.B., P.P. and G.E.H. wrote the article. H.B, G.E.H., P.P. and M.E.G. contributed to reviewing and/or editing of the manuscript before submission.

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Correspondence to Hilmar Bading.

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Hardingham, G., Pruunsild, P., Greenberg, M. et al. Lineage divergence of activity-driven transcription and evolution of cognitive ability. Nat Rev Neurosci 19, 9–15 (2018). https://doi.org/10.1038/nrn.2017.138

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