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Sensory experience regulates cortical inhibition by inducing IGF1 in VIP neurons
Open accessAbstract
Inhibitory neurons regulate the adaptation of neural circuits to sensory experience, but the molecular mechanisms by which experience controls the connectivity between different types of inhibitory neuron to regulate cortical plasticity are largely unknown. Here we show that exposure of dark-housed mice to light induces a gene program in cortical vasoactive intestinal peptide (VIP)-expressing neurons that is markedly distinct from that induced in excitatory neurons and other subtypes of inhibitory neuron. We identify Igf1 as one of several activity-regulated genes that are specific to VIP neurons, and demonstrate that IGF1 functions cell-autonomously in VIP neurons to increase inhibitory synaptic input onto these neurons. Our findings further suggest that in cortical VIP neurons, experience-dependent gene transcription regulates visual acuity by activating the expression of IGF1, thus promoting the inhibition of disinhibitory neurons and affecting inhibition onto cortical pyramidal neurons.
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“In contrast, neuronal activity induces a completely different transcriptional response in VIP+ interneurons, promoting the formation of inhibitory synapses on these cells (Mardinly et al., 2016).”
From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Mardinly et al., 2016
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“The AP-1 family and NPAS4 are transcription factors (TFs) that activate programs of gene transcription that are remarkably cell type specific (Mardinly et al., 2016; Spiegel et al., 2014; Vierbuchen et al., 2017) and thus tailored to the function of each neuronal subtype within the brain.”
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“To identify the subset of these genes likely to be induced by fear conditioning, we compared them to genes previously shown to be either activity-regulated in vitro 12 or induced upon first exposure to visual stimulus in the visual cortex 13 .”
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“…factor signaling each trigger specific programs of de novo transcription resulting in the up-regulation of highly selective and specific sets of target genes that modify neuronal wiring and function (Lambert et al , 2013; Spiegel et al , 2014; Mardinly et al , 2016; preprint: Russek et al , 2019).”
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“…studies have focused on the characteristics and functions of interneuron subtypes in the integration of various neural signals and the regulation of neuronal activity (Adesnik and Scanziani 2010; Adesnik et al. 2012; Pfeffer et al. 2013; Zhang et al. 2014; Neske et al. 2015; Mardinly et al. 2016).”
BackgroundMethodInfluentialCirculating Insulin-like Growth Factor I Regulates Its Receptor in the Brain of Male Mice
Trueba-Sáiz, Á., Fernandez, A. M., Nishijima, T., Mecha, M., Santi, A., Munive, V., & Torres‐Alemán, I. (2016) · Endocrinology · doi:10.1210/en.2016-1468 · Cited by 34
Tuning neural circuits by turning the interneuron knob
Dehorter, N., Marichal, N., Marín, Ó., & Berninger, B. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.12.009 · Cited by 34
Subregion-specific rules govern the distribution of neuronal immediate-early gene induction
Gonzales, B. J., Mukherjee, D., Ashwal-Fluss, R., Loewenstein, Y., & Citri, A. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1913658116 · Cited by 31
IGFBP2 Plays an Essential Role in Cognitive Development during Early Life
Khan, S., Lu, X., Huang, Q. D., Tang, J., Weng, J., Yang, Z., Lv, M., Xu, X., Xia, F., Zhang, M., et al. (2019) · Advanced Science · doi:10.1002/advs.201901152 · Cited by 31
Cell-type-specific programs for activity-regulated gene expression
Gray, J. M., & Spiegel, I. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.11.001 · Cited by 30
Neuropeptide signaling network of Caenorhabditis elegans: from structure to behavior
Watteyne, J., Chudinova, A., Ripoll-Sánchez, L., Schafer, W. R., & Beets, I. (2024) · Genetics · doi:10.1093/genetics/iyae141 · Cited by 36
“2012; Mardinly et al .”
Reduced insulin signaling maintains electrical transmission in a neural circuit in aging flies
Augustin, H., McGourty, K., Allen, M. J., Kudumala, S., Adcott, J., Kerr, F., Wong, C. T., Vincent, A. J., Godenschwege, T. A., Boucrot, E., et al. (2017) · PLoS Biology · doi:10.1371/journal.pbio.2001655 · Cited by 27
“For example, visual acuity in is improved in mice with reduced insulin signaling in the visual cortex [72].”
BackgroundHarris, N., Bates, S. G., Zhuang, Z., Bernstein, M., Stonemetz, J. M., Hill, T. J., Yu, Y. V., Calarco, J. A., & Sengupta, P. (2023) · Current Biology · doi:10.1016/j.cub.2023.02.073 · Cited by 30
The neuronal stimulation–transcription coupling map
Tyssowski, K. M., & Gray, J. M. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.05.001 · Cited by 28
Neuronal enhancers fine-tune adaptive circuit plasticity
Griffith, E. C., West, A. E., & Greenberg, M. E. (2024) · Neuron · doi:10.1016/j.neuron.2024.08.002 · Cited by 29
Carbone, B. E., Abouleish, M., Watters, K. E., Vogel, S., Ribic, A., Schroeder, O. H.-U., Bader, B. M., & Biederer, T. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz083 · Cited by 30
“1999; Sale et al. 2004; Ciucci et al. 2007; Mardinly et al. 2016).”
Neuronal activity-induced BRG1 phosphorylation regulates enhancer activation
Kim, B., Luo, Y., Zhan, X., Zhang, Z., Shi, X., Yi, J., Xuan, Z., & Wu, J. I. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109357 · Cited by 28
“The activity-induced expression of ARGs such as Arc, Bdnf, and Igf1 are important for synaptic maturation and homeostasis in various neuron subtypes (Hong et al., 2008; Jakkamsetti et al., 2013; Mardinly et al., 2016).”
BackgroundCell-type specific transcriptional adaptations of nucleus accumbens interneurons to amphetamine
Gallegos, D. A., Minto, M. S., Liu, F., Hazlett, M. F., Yousefzadeh, S. A., Bartelt, L. C., & West, A. E. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01466-1 · Cited by 24
Bayesian methods for event analysis of intracellular currents
Merel, J., Shababo, B., Naka, A., Adesnik, H., & Paninski, L. (2016) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2016.05.015 · Cited by 23
Fernandez, A. M., Hernández-Garzón, E., Guerrero‐Gómez, D., Miranda‐Vizuete, A., & Torres‐Alemán, I. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.08.034 · Cited by 24
Roles and Transcriptional Responses of Inhibitory Neurons in Learning and Memory
Giorgi, C., & Marinelli, S. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.689952 · Cited by 24
“These include epigenetic modulators, secreted factors and neuromodulators (Mardinly et al., 2016; Su et al., 2017; Hrvatin et al., 2018; Jaeger et al., 2018), responsible for translating the transcriptional response into a functional one and promoting cell-type specific cellular and synaptic changes at the circuit lev…”
BackgroundResultInfluentialCortical distribution of GABAergic interneurons is determined by migration time and brain size
Fazzari, P., Mortimer, N., Yabut, O., Vogt, D. L., & Pla, R. (2020) · Development · doi:10.1242/dev.185033 · Cited by 23
Zhang, L., Yue, Y., Ouyang, M., Liu, H., & Li, Z. (2017) · Neurochemical Research · doi:10.1007/s11064-017-2192-1 · Cited by 22
Pumo, G., Kitazawa, T., & Rijli, F. M. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.911023 · Cited by 23
“Similarly, a specific subclass of cortical inhibitory neurons shows a distinct LRG program which controls its ability to disinhibit cortical circuits (Mardinly et al., 2016).”
BackgroundResultIGF-1 receptor regulates upward firing rate homeostasis via the mitochondrial calcium uniporter
Katsenelson, M., Shapira, I., Abbas, E., Jevdokimenko, K., Styr, B., Ruggiero, A., Aïd, S., Fornasiero, E. F., Holzenberger, M., Rizzoli, S. O., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2121040119 · Cited by 23
“In the central nervous system, IGF1/IGF1R signaling is critical for experience-dependent synaptic and neuronal plasticity in sensory cortices (27-29), adult neurogenesis (30-32), synaptic vesicle release (33-35) (which was not certified by peer review) is the author/funder.”
BackgroundLocal autocrine plasticity signaling in single dendritic spines by insulin-like growth factors
Tu, X., Jain, A., Parra-Bueno, P., Decker, H., Liu, X., & Yasuda, R. (2023) · Science Advances · doi:10.1126/sciadv.adg0666 · Cited by 22
“Furthermore, aside from hippocampal pyramidal neurons, other types of brain cells, including γ-aminobutyric acid – releasing (GABAergic) and dopaminergic neurons as well as astrocytes, can synthesize IGF peptides and receive them through IGF1Rs ( 54 – 56 ).”
Brzdąk, P., Nowak, D., Wiera, G., & Mozrzymas, J. W. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00178 · Cited by 21
“Interestingly, the activity-dependent expression of ADAMTS-1 mRNA was found exclusively in somatostatin positive interneurons (Mardinly et al., 2016).”
BackgroundKetchesin, K. D., Huang, N. S., & Seasholtz, A. F. (2017) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2017.00090 · Cited by 22
“CRH is expressed in SST-, VIP- and VIP/CCK-expressing interneurons in the cortex, while CRH-R1 is localized in glutamatergic pyramidal neurons (Gallopin et al., 2006; Kubota et al., 2011; Refojo et al., 2011; Mardinly et al., 2016).”
BackgroundVisual processing mode switching regulated by VIP cells
Lee, J. H., & Mihalaş, Ş. (2017) · Scientific Reports · doi:10.1038/s41598-017-01830-0 · Cited by 22
Zimmer‐Bensch, G. (2018) · Brain Research · doi:10.1016/j.brainres.2018.09.001 · Cited by 22
Roethler, O., Zohar, E., Malina, K. C.-K., Bitan, L., Gabel, H. W., & Spiegel, I. (2023) · Neuron · doi:10.1016/j.neuron.2023.05.026 · Cited by 16
Yin, J., Gibbs, M., Long, C., Rosenthal, J., Kim, H. S., Kim, A., Sheng, C., Ding, P., Javed, U., & Yuan, Q. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.10.016 · Cited by 17
“Sensory experience also impacts mammalian cortical development by regulating the maturation rate and dendrite growth in inhibitory neurons (Chattopadhyaya et al., 2004; Mardinly et al., 2016).”
Neuregulin directed molecular mechanisms of visual cortical plasticity
Grieco, S. F., Holmes, T. C., & Xu, X. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24414 · Cited by 23
“…and extracellular matrix, and by synaptic molecules (Gu et al., 2013; Hanover et al., 1999; Huang et al., 1999; Kaneko & Stryker, 2017; Mardinly et al., 2016; Morishita, Miwa, Heintz, & Hensch, 2010; Pizzorusso et al., 2002, 2006; Putignano et al., 2007; Silingardi, Scali, Belluomini,…”
Holter, M. C., Hewitt, L. T., Nishimura, K. J., Knowles, S. J., Bjorklund, G. R., Shah, S., Fry, N., Rees, K. P., Gupta, T. A., Daniels, C. W., et al. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa413 · Cited by 22
“We have extended past cell-specific transcriptomic experiments to show that protein levels of ERK2 and MEK1 are lower in CINs than in surrounding PNs, which may be linked to the relative reduction in high P-ERK1/2-expressing CINs (Mardinly et al. 2016).”
BackgroundPostnatal Sox6 Regulates Synaptic Function of Cortical Parvalbumin-Expressing Neurons
Munguba, H., Chattopadhyaya, B., Nilsson, S., Carriço, J. N., Memic, F., Oberst, P., Batista‐Brito, R., Muñoz‐Manchado, A. B., Wegner, M., Fishell, G., et al. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0021-21.2021 · Cited by 19
“Activity-driven changes in gene expression vary across different neuronal subtypes (Mardinly et al., 2016) and different patterns and durations of stimuli can induce temporally distinct genetic programs (Tyssowski et al., 2018).”
BackgroundGoodwani, S., Fernandez, C., Acton, P. J., Buggia-Prévot, V., McReynolds, M. L., Ma, J., Hu, C. H., Hamby, M. E., Jiang, Y., Le, K., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21144849 · Cited by 19
“The physiological role of IGF1 pathway modulation requires further exploration, but could relate to synaptic modulation, as DLK regulates synaptic strength in multiple contexts [15,16] as does IGF1 [56].”
BackgroundInfluentialFiring Rate Homeostasis Can Occur in the Absence of Neuronal Activity-Regulated Transcription
Tyssowski, K. M., Letai, K. C., Rendall, S., Tan, C., Nizhnik, A., Kaeser, P. S., & Gray, J. M. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1108-19.2019 · Cited by 18
“Our manipulations of activity-regulated transcription likely prevent some alterations in E/I balance: homeostatic decreases in excitatory synaptic input onto excitatory neurons (Goold and Nicoll, 2010) are blocked by acute blockade of transcription, and KO experiments have demonstrated that homeostatic changes in inhi…”
BackgroundInfluentialThe neuropeptidergic connectome of C. elegansPreprint
Ripoll-Sánchez, L., Watteyne, J., Sun, H., Fernandez, R. W., Taylor, S. R., Weinreb, A., Hammarlund, M., Miller, D. M., Hobert, O., Beets, I., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.10.30.514396 · Cited by 21
Mastwal, S. S., Cao, V. Y., & Wang, K. H. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00100 · Cited by 16
“Particularly, it has been reported that neuronal activity induces distinctive gene expression programs in excitatory and inhibitory neurons (Spiegel et al., 2014; Mardinly et al., 2016).”
BackgroundMarin, I. A., Gutman-Wei, A. Y., Chew, K. S., Raissi, A. J., Djurisic, M. R., & Shatz, C. J. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2203965119 · Cited by 18
Yue, S., Wang, Y., & Wang, Z. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109204 · Cited by 19
“…neurons (Cao et al., 2011); vasoactive intestinal peptide (VIP)-expressing neuron-derived IGF1 increases inhibitory synaptic input onto VIP neurons (Mardinly et al., 2016) in visual cortex from young mice (P19–P21); and IGF1 reduces IPSC in ventromedial PFC layer V pyramidal neurons from young…”
Background
Metadata
- Authors
- Mardinly, A. R., Spiegel, I., Patrizi, A., Centofante, E., Bazinet, J. E., Tzeng, C. P., Mandel-Brehm, C., Harmin, D. A., Adesnik, H., Fagiolini, M., & Greenberg, M. E.
- Affiliations
- University of California, Berkeley (US)
- Harvard University (US)
- Boston Children's Hospital (US)
- Corresponding author
- Greenberg, M. E.
- ORCID
- Venue
- Nature
- Published
- 2016-03
- Volume
- 531
- Issue
- 7594
- Pages
- 371-375
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4823817
- OpenAlex
- W2293311540
- Cited by
- 176
- References
- 37
- Citations by year
- 2026: 6 · 2025: 22 · 2024: 12 · 2023: 14 · 2022: 18 · 2021: 17 · 2020: 13 · 2019: 23 · 2018: 19 · 2017: 20 · 2016: 12
- FWCI
- 13.83
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (P01NS047572, R01NS028829, R37NS028829)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P30HD018655)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Keywords
- insulin-like growth factor I, cortical inhibition, visual cortex, visual acuity, excitation-inhibition balance, light exposure, activity-dependent gene expression, inhibitory synaptic input, cortical plasticity, pyramidal neurons
- MeSH terms
- Animals, Female, Insulin-Like Growth Factor I, Male, Mice, Inbred C57BL, Neural Inhibition, Neural Pathways, Neuronal Plasticity, Neurons, Synapses, Vasoactive Intestinal Peptide, Vision, Ocular, Visual Cortex, Pyramidal Cells, Mice
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