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Npas4 Regulates Excitatory-Inhibitory Balance within Neural Circuits through Cell-Type-Specific Gene Programs

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Spiegel, Ivo, Mardinly, Alan R., Gabel, Harrison W., Bazinet, Jeremy E., Couch, Cameron H., Tzeng, Christopher P., Harmin, David A., Greenberg, Michael E.·2014·Cell

DOI 10.1016/j.cell.2014.03.058PMC PMC4089405

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Abstract

The nervous system adapts to experience by inducing a transcriptional program that controls important aspects of synaptic plasticity. Although the molecular mechanisms of experience-dependent plasticity are well characterized in excitatory neurons, the mechanisms that regulate this process in inhibitory neurons are only poorly understood. Here, we describe a transcriptional program that is induced by neuronal activity in inhibitory neurons. We find that, while neuronal activity induces expression of early-response transcription factors such as Npas4 in both excitatory and inhibitory neurons, Npas4 activates distinct programs of late-response genes in inhibitory and excitatory neurons. These late-response genes differentially regulate synaptic input to these two types of neurons, promoting inhibition onto excitatory neurons while inducing excitation onto inhibitory neurons. These findings suggest that the functional outcomes of activity-induced transcriptional responses are adapted in a cell-type-specific manner to achieve a circuit-wide homeostatic response.

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Background
NMDARs regulate the excitatory-inhibitory balance within neural circuits
Zhou, L., Sun, X., & Duan, J. (2023) · Brain Science Advances · doi:10.26599/bsa.2022.9050020 · Cited by 7
“cell type-specific activity-dependent manner [70].”
Adolescent chronic intermittent toluene inhalation dynamically regulates the transcriptome and neuronal methylome within the rat medial prefrontal cortex
Dick, A. L. W., Zhao, Q., Crossin, R., Baker‐Andresen, D., Li, X., Edson, J., Roeh, S., Marshall, V., Bredy, T. W., Lawrence, A. J., et al. (2020) · Addiction Biology · doi:10.1111/adb.12937 · Cited by 7
TAF15 Overexpression Impairs Memory in Mice by Inhibiting the Transcription of Npas4
Ding, M., Li, D., Zhang, J., & Liu, Q. (2024) · Neuroscience Bulletin · doi:10.1007/s12264-024-01273-4 · Cited by 5
“NPTX2 (the protein encoded by the Nptx2 gene) is colocalized with PSD95 at excitatory synapses, and overexpression of NPTX2 leads to an increase in the number of synapses in spinal neurons [9, 10].”
Neuronal type-specific modulation of cognition and AP-1 signaling by early-life rearing conditions
Alaiz-Noya, M., Miozzo, F., Fuentes-Ramos, M., Machnicka, M. A., Kurowska, M., Herrera, M. L., del Blanco, B., Niñerola, S., Bustos-Martínez, I., Wilczyński, B., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-65343-5 · Cited by 6
Disrupted synapses: prefrontal cortex-reward circuit dysfunction in stress-induced depression-like behaviors
Mahmud, A., & Karaman, M. A. (2026) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2026.1843871 · Cited by 7
“…NPAS4 is linked to cellular and microcircuit processes that regulate the balance of E/I ratio, mediating an adaptive plasticity mechanism in which high levels of neuronal excitation trigger the formation of new inhibitory synapses on the excited cells (Spiegel et al., 2014; Ye et al., 2016).”
A comprehensive protocol for efficient differentiation of human NPCs into electrically competent neurons
Romito, E., Battistella, I., Plakhova, V. B., Paplekaj, A., Forastieri, C., Toffolo, E., Musio, C., Conti, L., Battaglioli, E., & Rusconi, F. (2024) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2024.110225 · Cited by 6
“…plays a role in a plethora of cell types, responding to proliferation signals in non-neuronal cells (Cruz-Mendoza et al., 2022), Npas4 is only expressed in excitatory and inhibitory neurons, being its function only dedicated to neuroplasticity regulation (Sun and Lin, 2016; Spiegel et al., 2014).”
Background
Molecular mechanisms underlying activity-dependent ischemic tolerance in the brain
Takahashi, H., Yamamoto, T., & Tsuboi, A. (2022) · Neuroscience Research · doi:10.1016/j.neures.2022.10.005 · Cited by 6
Theanine, a Tea-Leaf-Specific Amino Acid, Alleviates Stress through Modulation of Npas4 Expression in Group-Housed Older Mice
Unno, K., Taguchi, K., Konishi, T., Ozeki, M., & Nakamura, Y. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24043983 · Cited by 6
Integration of whole-exome sequencing and structural neuroimaging analysis in major depressive disorder: a joint study
Oh, E.-Y., Han, K., Kim, A., Kang, Y., Tae, W., Han, M.-R., & Ham, B. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-02849-4 · Cited by 8
“More detailed or raw data from the current study are available from the corresponding author upon reasonable request.”
Background
Effects of Propofol General Anesthesia on Olfactory Relearning
Jia, L., Tang, P. S., Brandon, N. R., Luo, Y., Yu, B., & Xu, Y. (2016) · Scientific Reports · doi:10.1038/srep33538 · Cited by 8
Optogenetic stimulation of a cortical biohybrid implant guides goal directed behaviorPreprint
Brown, J., Zappitelli, K. M., Dawson, P. M., Yoon, E., Shiraga, S., Rochford, A. E., Eltaeb, M., Rodriguez, A., Kong, Y., Hodak, M., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.22.624907 · Cited by 7
CRISPR-Cas9-generated PTCHD1 2489T>G stem cells recapitulate patient phenotype when undergoing neural induction
Farley, K. O., Forbes, C. A., Shaw, N. C., Kuzminski, E., Ward, M., Baynam, G., Lassmann, T., & Fear, V. S. (2024) · Human Genetics and Genomics Advances · doi:10.1016/j.xhgg.2023.100257 · Cited by 5
Chromatin regulation of neuronal activity-dependent gene programs in circuit formation and plasticity
Pumo, G., & Rijli, F. M. (2025) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2025.103024 · Cited by 5
NPAS4 Depletion in POMC Neurons Protects From Obesity and Alters the Feeding-regulated Transcriptome in Male Mice
Yoon, J. S., Gamu, D., Gibson, W. T., & Lynn, F. C. (2025) · Endocrinology · doi:10.1210/endocr/bqaf083 · Cited by 4
“At the molecular level, Npas4 regulates the inhibitory-excitatory balance within neural circuits by activating distinct cell type–specific gene sets, which includes its downstream target brain-derived neurotrophic factor (10-12).”
The elusive transcriptional memory trace
Gil-Martí, B., Barredo, C. G., Pina-Flores, S., Trejo, J. L., Turiégano, E., & Martín, F. A. (2022) · Oxford Open Neuroscience · doi:10.1093/oons/kvac008 · Cited by 5
“Until recently, the consensus view was that there was a common set of IEGs that induces differential expression of LRGs,depending on the neuronal subtype [47].”
Background
Non-Invasive Assessment of Neurogenesis Dysfunction in Fetuses with Early-Onset Growth Restriction Using Fetal Neuronal Exosomes Isolating from Maternal Blood: A Pilot Study
Gusar, V. A., Кан, Н. Е., Leonova, A., Chagovets, V., Tyutyunnik, V., Khachatryan, Z. V., Львовна, Я. Е., & Sukhikh, G. T. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26041497 · Cited by 5
“The clinical data of patients are presented in Table 1.”
Protein Kinase A-Dependent Plasticity of Local Inhibitory Synapses from Hilar Somatostatin-Expressing Neurons
Hernández‐Vivanco, A., Jiménez-Redondo, E., Cano-Adamuz, N., & Méndez, P. (2023) · eNeuro · doi:10.1523/eneuro.0089-23.2023 · Cited by 5
“In addition, INs are exquisitely sensitive to different forms of neuronal activity that activate multiple signaling pathways resulting in changes in gene expression, synapse structure, and efficacy (Spiegel et al., 2014).”
Background
Developmental dysfunction in a preclinical model of Kcnq2 developmental and epileptic encephalopathy
Mao, M., Jancovski, N., Kushner, Y., Teasdale, L., Truong, P. H., Zhou, K., Reid, S., Jia, L., Aung, Y. H., Li, M., et al. (2024) · Neurobiology of Disease · doi:10.1016/j.nbd.2024.106782 · Cited by 6
“…resulted from differentially expressed ion detected at P12 which gradually but permanently altered the developmental of neurons and their connectome. promoting GABAergic synaptic formation onto excitatory neurons and feedback inhibition in neuronal circuits (Lin et al., 2008; Spiegel et al., 2014).”
Translatome Analyses Using Conditional Ribosomal Tagging in GABAergic Interneurons and Other Sparse Cell Types
Mahadevan, V., Peltekian, A., & McBain, C. J. (2020) · Current Protocols in Neuroscience · doi:10.1002/cpns.93 · Cited by 5
“To circumvent the caveats associated with polysome integrity loss result- ing from freezing the tissue, some studies have pooled the tissue from multiple animals to gain enough “mRNA material” for downstream analysis (Mardinly et al., 2016; Spiegel et al., 2014).”
Background
Spatiotemporal Mapping and Molecular Basis of Whole-brain Circuit MaturationPreprint
Xue, J., Brawner, A. T., Thompson, J. R., Yelhekar, T. D., Newmaster, K. T., Qiu, Q., Cooper, Y. A., Yu, C. R., Ahmed-Braima, Y. H., Kim, Y., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.01.03.572456 · Cited by 5
Molecular and genetic mechanisms of plasticity in addiction
Brida, K. L., & Day, J. J. (2025) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2025.103032 · Cited by 4
“Similar to its role in regulating excitatory/ inhibitory balance in other brain regions [59], the effects of Npas4 seem tied to regulation of activity balance be-tween D1-and D2-MSNs, with knockdown increasing both PFC connectivity to D2-MSNs and the ratio of D2:D1 Fos þ neurons following cocaine…”
Loss of REST associated with Alzheimer's disease pathology is ameliorated by NAD+
Lagartos-Donate, M. J., Escobar-Doncel, B., Zhang, S.-Q., Pan, J., González, N., Anisimov, A. S., Montaldo, N. P., Jensen, V., Mao, L., Li, B., et al. (2025) · Brain · doi:10.1093/brain/awaf261 · Cited by 5
“52 Additionally, upregulation of REST in the HIP led to changes in mRNA expression of genes involved in pathways important for neuronal survival and function, such as endo-lysosomal pathway, oxidative stress and chromatin remodelling (Fig.”
Female rat transcriptome response to infraorbital nerve transection differs from that of males: RNA‐seq
Orczyk, J. J., Batka, R. J., Gore, A., Maio-lexa, M., Kulkarni, A., & Garraghty, P. E. (2016) · The Journal of Comparative Neurology · doi:10.1002/cne.24045 · Cited by 4
“The net result is an increase in inhibition of circuit activity through increasing GABA release (Spiegel et al., 2014).”
Background
Inhibition of spreading depolarizations by targeting GABAA receptors and voltage‐gated sodium channels improves neurological deficits in rats with traumatic brain injury
Yan, R., Liu, Q., Zhang, D., Li, K., Li, Y., Nie, Y., Zhang, Y., Li, P., Mao, S., & Li, H. (2025) · British Journal of Pharmacology · doi:10.1111/bph.70117 · Cited by 4
“This process also determines the number of functional GABAergic synapses (Spiegel et al., 2014).”
Lack of Stim2 Affects Vision-Dependent Behavior and Sensitivity to Hypoxia
Wasilewska, I., Majewski, Ł., Adamek‐Urbańska, D., Mondal, S. S., Baranykova, S., Gupta, R. K., Bielecki, D., Winata, C. L., & Kuźnicki, J. (2023) · Zebrafish · doi:10.1089/zeb.2022.0068 · Cited by 4
“61,62 65 Thus, Stim2 may participate in the regulation of neurotransmission by affecting the expression of synapse components.”
Effect of Short-Term Restraint Stress on the Hypothalamic Transcriptome Profiles of Rats with Inherited Stress-Induced Arterial Hypertension (ISIAH) and Normotensive Wistar Albino Glaxo (WAG) Rats
Oshchepkov, D. Y., Makovka, Y. V., Fedoseeva, L. A., Seryapina, A. A., Markel, А. L., & Redina, O. E. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25126680 · Cited by 6
“Accordingly, Npas4 is considered as an early-response TF that regulates the expression of inhibitory synapse genes to control homeostatic excitatory/inhibitory balance in neurons [36,37].”
Background
Activity-dependent transcriptional programs in memory regulate motor recovery after stroke
Joy, M. T., & Carmichael, S. T. (2024) · Communications Biology · doi:10.1038/s42003-024-06723-3 · Cited by 4
Structural insights and characterization of human Npas4 protein
Fahim, A., Rehman, Z., Bhatti, M. F., Ali, A., Virk, N., Rashid, A., & Paracha, R. Z. (2018) · PeerJ · doi:10.7717/peerj.4978 · Cited by 4
Transcriptome analysis of hippocampal subfields identifies gene expression profiles associated with long-term active place avoidance memoryPreprint
Harris, R. M., Kao, H., Alarcón, J. M., Fenton, A. A., & Hofmann, H. A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.02.05.935759 · Cited by 4
“Neuro6d was the only transcription factor that showed decreased expression, whereas Npas4, which is thought to mediate learning-related plasticity, especially of neural inhibition (Lin et al., 2008; Spiegel et al., 2014; Weng et al., 2018) was more highly expressed in the DG.”
Background
NMDAR-mediated transcriptional control of gene expression during the development of medial ganglionic eminence-derived interneuronsPreprint
Mahadevan, V., Mitra, A., Zhang, Y., Yuan, X. Q., Peltekian, A., Chittajallu, R., Esnault, C., Maric, D., Rhodes, C. T., Pelkey, K. A., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.10.144295 · Cited by 4
NPAS4 supports drug-cue associations and relapse-like behavior through regulation of the cell type-specific activation balance in the nucleus accumbensPreprint
Hughes, B. W., Tsvetkov, E., Siemsen, B. M., Snyder, K. K., Akiki, R. M., Wood, D. J., Penrod, R. D., Scofield, M. D., Berto, S., Taniguchi, M., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.09.04.506434 · Cited by 4
Stimulus-Dependent Expression of Bdnf Is Mediated by ATF2, MYT1L, and EGR1 Transcription Factors
Esvald, E., Moistus, A., Lehe, K., Avarlaid, A., Shubina, A., Kuusemets, L., Tuvikene, J., & Timmusk, T. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.0313-24.2025 · Cited by 4
Single-cell multiomics of neuron activation reveals context-specific genetics of brain disorders
Liang, L., Zhang, S., Wang, Z., Zhang, H., Li, C., Thapa, C., Oh, E., Sirkin, D., Sun, X., Barishman, A., et al. (2026) · Science · doi:10.1126/science.adw3949 · Cited by 3
Berberine protects against chronic social defeat stress-induced depressive-like behaviors with upregulation of neuronal PAS domain protein 4/brain-derived neurotrophic factor signaling pathway
Gao, W., Deng, Z., & Peng, Y. (2018) · Pharmacognosy Magazine · doi:10.4103/pm.pm_268_18 · Cited by 4
Meso-seq for in-depth transcriptomics in ultra-low amounts of FACS-purified neuronal nuclei
Apelblat, D., Roethler, O., Bitan, L., Keren‐Shaul, H., & Spiegel, I. (2022) · Cell Reports Methods · doi:10.1016/j.crmeth.2022.100259 · Cited by 3
Enhancement of physiology via adaptive transcription
Lissek, T. (2024) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-024-03037-5 · Cited by 3
“…different down-stream effects in different cell types which is important with regard to cell tropism in AAV-based deliveries (e.g., Npas4 controls different gene programs in excitatory vs. inhibitory neurons with resulting differential effects on excitatory and inhibitory input onto cells [84]).”
The Impact of Ecological Niche on Adaptive Flexibility of Sensory Circuitry
Pallas, S. L. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00344 · Cited by 4
“This signaling pathway promotes BDNF transcription, leading to TrkB-mediated alterations in GABAergic inhibition (Hong et al., 2008; Lin et al., 2008; Bloodgood et al., 2013; Park and Poo, 2013; Spiegel et al., 2014).”
Background
Transcriptional and Epigenetic Regulation of Reward Circuitry in Drug Addiction
Eagle, A. L., Klump, B. M., & Robison, A. J. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-812202-0.00003-8 · Cited by 4
Dysregulation ofNpas4andInhbaexpression and an altered excitation–inhibition balance are associated with cognitive deficits in DBA/2 micePreprint
Oberländer, K., Witte, V., Mallien, A. S., Gass, P., Bengtson, C. P., & Bading, H. (2022) · Learning & Memory · doi:10.1101/lm.053527.121 · Cited by 3
“…long-term potentiation in CA1 pyramidal neurons (Ageta et al. 2010; Hasegawa et al. 2014) andNpas4 expression regulates both excitatory and inhibitory synaptic connectivity in the hippocampus (Lin et al. 2008; Sim et al. 2013; Spiegel et al. 2014), we next investigated synaptic function in the CA1.”
BackgroundInfluential
Core and Flanking bHLH-PAS:DNA interactions mediate specificity and drive obesityPreprint
Bersten, D. C., Sullivan, A. E., McDougal, D. P., Breen, J., Fitzsimmons, R. L., Muscat, G. E. O., Pederson, S., Bruning, J. B., Fan, C., Thomas, P., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.02.01.475276 · Cited by 3
Activity-dependent expression of Fezf2 regulates inhibitory synapse formation in pyramidal cellsPreprint
Kroon, T., Sanalidou, S., Maeso, P. A., Garcés, T., Yang, H., & Rico, B. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.01.11.575171 · Cited by 3
lncRNA ADEPTR loss-of-function elicits sex-specific behavioral and spine deficits
Chanda, K., Carter, J. P., Nishizono, H., Raveendra, B., Brantley, A. F., Grinman, E., Espadas, I., Lozano-Villada, S., Wingfield, J. L., Wagner, G., et al. (2025) · iScience · doi:10.1016/j.isci.2025.113070 · Cited by 2
“Surprisingly, both S-ADEPTR and L-ADEPTR KO mice displayed no significant memory deficits across multiple tasks, including NOR, MWM, SA, and CFC/TFC (Figures 2, 3, and S1–S5).”
Chromatin Remodelers in Neuronal Gene Transcription
Cornejo, K. G., & Saha, R. N. (2024) · Springer eBooks · doi:10.1007/978-3-031-68550-7_9 · Cited by 2
Identification of Npas4 as a biomarker for CICI by transcriptomics combined with bioinformatics and machine learning approaches
He, Z., Ma, H., Zhang, Y., Chen, L., Pang, Y., Ding, X., Wang, Y., Liu, Y., Li, L., & Li, J. (2025) · Experimental Neurology · doi:10.1016/j.expneurol.2025.115290 · Cited by 2
Serum Npas-4 and Nptx-2 Levels in Alzheimer’s Disease: Potential Biomarkers of Synaptic Dysfunction in a Cross-Sectional Study
Özkaya, A. L., Gürbüzer, N., Mercantepe, T., & Mercantepe, F. (2025) · Biomolecules · doi:10.3390/biom15060795 · Cited by 3

Authors: Spiegel, I., Mardinly, A. R., Gabel, H. W., Bazinet, J. E., Couch, C. H., Tzeng, C. P., Harmin, D. A., & Greenberg, M. E.
Affiliations: Harvard University (US)
Corresponding author: Greenberg, Michael E.
ORCID: Spiegel, Ivo
Mardinly, Alan R.
Gabel, Harrison W.
Tzeng, Christopher P.
Greenberg, Michael E.
Venue: Cell
Publisher: Elsevier BV
Published: 2014-05
Volume: 157
Issue: 5
Pages: 1216-1229
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2014.03.058
PMC: PMC4089405
OpenAlex: W2079540311
Cited by: 416
References: 52
Citations by year: 2026: 31 · 2025: 49 · 2024: 41 · 2023: 28 · 2022: 38 · 2021: 37 · 2020: 29 · 2019: 34 · 2018: 31 · 2017: 32 · 2016: 34 · 2015: 23 · 2014: 8
FWCI: 14.77
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 414 d)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (5r01ns048276-15)
National Institute of Mental Health (T32MH020017)
National Institute of Neurological Disorders and Stroke (R01NS028829, NS048276, 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 › Cognitive Neuroscience › Neural dynamics and brain function
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: Npas4, excitation-inhibition balance, inhibitory neurons, excitatory neurons, activity-dependent transcription, synaptic plasticity, homeostatic regulation, neural circuits
MeSH terms: Animals, Embryo, Mammalian, Gene Expression Regulation, Neurons, Synapses, Transcription, Genetic, Mice, Knockout, Cell Culture Techniques, Mice, Basic Helix-Loop-Helix Proteins

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Npas4 Regulates Excitatory-Inhibitory Balance within Neural Circuits through Cell-Type-Specific Gene Programs

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