Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Neurogliaform cells in cortical circuits

Nature Reviews Neuroscience volume 16, pages 458–468 (2015)Cite this article

Subjects

Key Points

  • Neurogliaform cells are a novel subtype of hippocampal and cortical local-circuit GABAergic inhibitory interneuron that primarily reside within the superficial layers of the cortex and hippocampal formations.

  • This comparatively small cell type has both dendrites and axons that remain relatively local to the cell body forming a dense plexus that is highly interconnected with other neurogliaform cells through both chemical and electrical synapses.

  • Anatomical and electrophysiological studies indicate that the axons of these cells have an unusually high presynaptic bouton density and are spatially located at larger than usual distances from their postsynaptic targets. This arrangement suggests that they communicate via a hybrid form of inhibitory synaptic transmission intermediate between phasic and tonic forms of inhibition that lacks target cell specificity

  • NGF cells contain numerous neuroactive petides and compounds such as neuropeptide Y, reelin neuronal nitric oxide synthase and insulin that may all serve important functional roles in regulating the neuronal circuits in which they are embedded.

  • Local circuit GABAergic interneurons have numerous roles in regulating neuronal oscillatory activity. The low-frequency firing of neurogliaform (NGF) cells provide temporally slow GABAergic inputs onto specific pyramidal cell domains suggesting that they contribute to theta rhythms as well as theta-frequency modulation of gamma oscillations

  • The early appearance of NGF cells in the developing cortex makes NGF cells attractive candidates for providing trophic GABA signalling cues to both developing and adult-born glutamatergic principal cells.

Abstract

Recent research into local-circuit GABAergic inhibitory interneurons of the mammalian central nervous system has provided unprecedented insight into the mechanics of neuronal circuitry and its dysfunction. Inhibitory interneurons consist of a broad array of anatomically and neurochemically diverse cell types, and this suggests that each occupies an equally diverse functional role. Although neurogliaform cells were observed by Cajal over a century ago, our understanding of the functional role of this class of interneurons is in its infancy. However, it is rapidly becoming clear that this cell type operates under a distinct repertoire of rules to provide novel forms of inhibitory control of numerous afferent pathways.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Diversity of neurogliaform cell morphology.
Figure 2: Anatomical and electrophysiological characterization of nNOS-negative and nNOS-positive CA1 hippocampal NGF cells.
Figure 3: Distinct forms of signalling generate diverse GABA receptor-mediated responses.
Figure 4: Two examples of how CA1 stratum lucidum NGF cells may act as a global gate for afferent information flow.
Figure 5: NGF cells coordinate activity in the neurogenic adult dentate gyrus.

Similar content being viewed by others

References

  1. Klausberger, T. & Somogyi, P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321, 53–57 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. McBain, C. J. & Fisahn, A. Interneurons unbound. Nat. Rev. Neurosci. 2, 11–23 (2001).

    CAS  PubMed  Google Scholar 

  3. Bezaire, M. J. & Soltesz, I. Quantitative assessment of CA1 local circuits: knowledge base for interneuron–pyramidal cell connectivity. Hippocampus 23, 751–785 (2013). A comprehensive review providing quantification of interneuron cell types and their connectivity within cortical circuits.

    PubMed  PubMed Central  Google Scholar 

  4. Roux, L. & Buzsaki, G. Tasks for inhibitory interneurons in intact brain circuits. Neuropharmacology 88, 10–23 (2014).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  6. Ramón y Cajal, S. Histology of the Nervous System of Man and Vertebrates (Oxford University Press, 1995).

    Google Scholar 

  7. Lacaille, J. C. & Schwartzkroin, P. A. Stratum lacunosum-moleculare interneurons of hippocampal CA1 region. II. Intrasomatic and intradendritic recordings of local circuit synaptic interactions. J. Neurosci. 8, 1411–1424 (1988). An image in this paper may be the first of a filled NGF cell recorded in the CA1 stratum lacunosum moleculare.

    CAS  PubMed  Google Scholar 

  8. Price, C. J. et al. Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. J. Neurosci. 25, 6775–6786 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Khazipov, R., Congar, P. & Ben-Ari, Y. Hippocampal CA1 lacunosum-moleculare interneurons: modulation of monosynaptic GABAergic IPSCs by presynaptic GABAB receptors. J. Neurophysiol. 74, 2126–2137 (1995).

    CAS  PubMed  Google Scholar 

  10. Vida, I., Halasy, K., Szinyei, C., Somogyi, P. & Buhl, E. H. Unitary IPSPs evoked by interneurons at the stratum radiatum–stratum lacunosum-moleculare border in the CA1 area of the rat hippocampus in vitro. J. Physiol. 506, 755–773 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Miyoshi, G. et al. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J. Neurosci. 30, 1582–1594 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Fuentealba, P. et al. Ivy cells: a population of nitric-oxide-producing, slow-spiking GABAergic neurons and their involvement in hippocampal network activity. Neuron 57, 917–929 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Tricoire, L. et al. Common origins of hippocampal ivy and nitric oxide synthase expressing neurogliaform cells. J. Neurosci. 30, 2165–2176 (2010). This study shows that unlike cortical NGF cells which originate within the caudal ganglionic eminence, hippocampal NGF have their origins in both the medial and caudal ganglionic eminences.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Tricoire, L. et al. A blueprint for the spatiotemporal origins of mouse hippocampal interneuron diversity. J. Neurosci. 31, 10948–10970 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Somogyi, J., Szabo, A., Somogyi, P. & Lamsa, K. Molecular analysis of ivy cells of the hippocampal CA1 stratum radiatum using spectral identification of immunofluorophores. Front. Neural Circuits 6, 35 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Jiang, X., Wang, G., Lee, A. J., Stornetta, R. L. & Zhu, J. J. The organization of two new cortical interneuronal circuits. Nat. Neurosci. 16, 210–218 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Munoz-Manchado, A. B. et al. Novel striatal GABAergic interneuron populations labeled in the 5HT3aEGFP mouse. Cereb. Cortex http://dx.doi.org/10.1093/cercor/bhu179 (2014).

  18. Armstrong, C., Szabadics, J., Tamas, G. & Soltesz, I. Neurogliaform cells in the molecular layer of the dentate gyrus as feed-forward gamma-aminobutyric acidergic modulators of entorhinal–hippocampal interplay. J. Comp. Neurol. 519, 1476–1491 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Armstrong, C., Krook-Magnuson, E. & Soltesz, I. Neurogliaform and ivy cells: a major family of nNOS expressing GABAergic neurons. Front. Neural Circuits 6, 23 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Fuentealba, P. et al. Expression of COUP-TFII nuclear receptor in restricted GABAergic neuronal populations in the adult rat hippocampus. J. Neurosci. 30, 1595–1609 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Sik, A., Penttonen, M., Ylinen, A. & Buzsaki, G. Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J. Neurosci. 15, 6651–6665 (1995).

    CAS  PubMed  Google Scholar 

  22. De Marco Garcia, N. V., Karayannis, T. & Fishell, G. Neuronal activity is required for the development of specific cortical interneuron subtypes. Nature 472, 351–355 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. De Marco Garcia, N. V., Priya, R., Tuncdemir, S. N., Fishell, G. & Karayannis, T. Sensory inputs control the integration of neurogliaform interneurons into cortical circuits. Nat. Neurosci. 18, 393–401 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Olah, S. et al. Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature 461, 1278–1281 (2009). This study provides anatomical and physiological evidence that NGF cells release GABA into the extracellular space to provide a mode of inhibition that lacks spatial selectivity.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Quattrocolo, G. & Maccaferri, G. Novel GABAergic circuits mediating excitation/inhibition of Cajal-Retzius cells in the developing hippocampus. J. Neurosci. 33, 5486–5498 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Capogna, M. & Pearce, R. A. GABAA,slow: causes and consequences. Trends Neurosci. 34, 101–112 (2011).

    CAS  PubMed  Google Scholar 

  27. Kawaguchi, Y. Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J. Neurosci. 15, 2638–2655 (1995).

    CAS  PubMed  Google Scholar 

  28. Chikwendu, A. & McBain, C. J. Two temporally overlapping “delayed-rectifiers” determine the voltage-dependent potassium current phenotype in cultured hippocampal interneurons. J. Neurophysiol. 76, 1477–1490 (1996).

    CAS  PubMed  Google Scholar 

  29. Zhang, L. & McBain, C. J. Potassium conductances underlying repolarization and after-hyperpolarization in rat CA1 hippocampal interneurones. J. Physiol. 488, 661–672 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Zhang, L. & McBain, C. J. Voltage-gated potassium currents in stratum oriens-alveus inhibitory neurones of the rat CA1 hippocampus. J. Physiol. 488, 647–660 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Morin, F., Haufler, D., Skinner, F. K. & Lacaille, J. C. Characterization of voltage-gated K+ currents contributing to subthreshold membrane potential oscillations in hippocampal CA1 interneurons. J. Neurophysiol. 103, 3472–3489 (2010).

    CAS  PubMed  Google Scholar 

  32. Atzori, M. et al. H2 histamine receptor-phosphorylation of Kv3.2 modulates interneuron fast spiking. Nat. Neurosci. 3, 791–798 (2000).

    CAS  PubMed  Google Scholar 

  33. Weiser, M. et al. Differential expression of Shaw-related K+ channels in the rat central nervous system. J. Neurosci. 14, 949–972 (1994).

    CAS  PubMed  Google Scholar 

  34. Sheffield, M. E., Best, T. K., Mensh, B. D., Kath, W. L. & Spruston, N. Slow integration leads to persistent action potential firing in distal axons of coupled interneurons. Nat. Neurosci. 14, 200–207 (2011).

    CAS  PubMed  Google Scholar 

  35. Sheffield, M. E. et al. Mechanisms of retroaxonal barrage firing in hippocampal interneurons. J. Physiol. 591, 4793–4805 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Krook-Magnuson, E., Luu, L., Lee, S. H., Varga, C. & Soltesz, I. Ivy and neurogliaform interneurons are a major target of μ-opioid receptor modulation. J. Neurosci. 31, 14861–14870 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Suzuki, N., Tang, C. S. & Bekkers, J. M. Persistent barrage firing in cortical interneurons can be induced in vivo and may be important for the suppression of epileptiform activity. Front. Cell Neurosci. 8, 76 (2014).

    PubMed  PubMed Central  Google Scholar 

  38. Takacs, V. T., Klausberger, T., Somogyi, P., Freund, T. F. & Gulyas, A. I. Extrinsic and local glutamatergic inputs of the rat hippocampal CA1 area differentially innervate pyramidal cells and interneurons. Hippocampus 22, 1379–1391 (2012).

    CAS  PubMed  Google Scholar 

  39. Matta, J. A. et al. Developmental origin dictates interneuron AMPA and NMDA receptor subunit composition and plasticity. Nat. Neurosci. 16, 1032–1041 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Quattrocolo, G. & Maccaferri, G. Optogenetic activation of Cajal-Retzius cells reveals their glutamatergic output and a novel feedforward circuit in the developing mouse hippocampus. J. Neurosci. 34, 13018–13032 (2014). This study shows a novel monosynaptic connection between reelin-positive Cajal–Retzius cells and NGF cells within the CA1 hippocampus.

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Williams, S., Samulack, D. D., Beaulieu, C. & LaCaille, J. C. Membrane properties and synaptic responses of interneurons located near the stratum lacunosum-moleculare/radiatum border of area CA1 in whole-cell recordings from rat hippocampal slices. J. Neurophysiol. 71, 2217–2235 (1994).

    CAS  PubMed  Google Scholar 

  42. Olah, S. et al. Output of neurogliaform cells to various neuron types in the human and rat cerebral cortex. Front. Neural Circuits 1, 4 (2007).

    PubMed  PubMed Central  Google Scholar 

  43. Karayannis, T. et al. Slow GABA transient and receptor desensitization shape synaptic responses evoked by hippocampal neurogliaform cells. J. Neurosci. 30, 9898–9909 (2010). This study quantifies the low and prolonged GABA concentration profile produced by NGF cells in the hippocampus.

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Overstreet, L. S., Jones, M. V. & Westbrook, G. L. Slow desensitization regulates the availability of synaptic GABAA receptors. J. Neurosci. 20, 7914–7921 (2000).

    CAS  PubMed  Google Scholar 

  45. Tamas, G., Lorincz, A., Simon, A. & Szabadics, J. Identified sources and targets of slow inhibition in the neocortex. Science 299, 1902–1905 (2003).

    CAS  PubMed  Google Scholar 

  46. Szabadics, J., Tamas, G. & Soltesz, I. Different transmitter transients underlie presynaptic cell type specificity of GABAA,slow and GABAA,fast . Proc. Natl Acad. Sci. USA 104, 14831–14836 (2007). This study shows that slow IPSCs generated by NGF cells in the cortex have characteristics of spillover-mediated transmission.

    CAS  PubMed  Google Scholar 

  47. Markwardt, S. J., Dieni, C. V., Wadiche, J. I. & Overstreet-Wadiche, L. Ivy/neurogliaform interneurons coordinate activity in the neurogenic niche. Nat. Neurosci. 14, 1407–1409 (2011). This study shows that newly generated adult-born neurons respond to GABA released by single NGF cells.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Isaacson, J. S., Solis, J. M. & Nicoll, R. A. Local and diffuse synaptic actions of GABA in the hippocampus. Neuron 10, 165–175 (1993).

    CAS  PubMed  Google Scholar 

  49. Scanziani, M. GABA spillover activates postsynaptic GABAB receptors to control rhythmic hippocampal activity. Neuron 25, 673–681 (2000).

    CAS  PubMed  Google Scholar 

  50. Price, C. J., Scott, R., Rusakov, D. A. & Capogna, M. GABAB receptor modulation of feedforward inhibition through hippocampal neurogliaform cells. J. Neurosci. 28, 6974–6982 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Chittajallu, R., Pelkey, K. A. & McBain, C. J. Neurogliaform cells dynamically regulate somatosensory integration via synapse-specific modulation. Nat. Neurosci. 16, 13–15 (2013). This study provides the exception to the rule that all NGF cells lack specificity in their innervation of postsynaptic targets.

    CAS  PubMed  Google Scholar 

  52. Cauli, B. et al. Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J. Neurosci. 24, 8940–8949 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Li, G., Stewart, R., Canepari, M. & Capogna, M. Firing of hippocampal neurogliaform cells induces suppression of synaptic inhibition. J. Neurosci. 34, 1280–1292 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Molnar, G. et al. GABAergic neurogliaform cells represent local sources of insulin in the cerebral cortex. J. Neurosci. 34, 1133–1137 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Jarsky, T., Roxin, A., Kath, W. L. & Spruston, N. Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nat. Neurosci. 8, 1667–1676 (2005).

    CAS  PubMed  Google Scholar 

  56. Colbert, C. M. & Levy, W. B. Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by glutamate receptors. J. Neurophysiol. 68, 1–8 (1992).

    CAS  PubMed  Google Scholar 

  57. Rudy, B., Fishell, G., Lee, S. & Hjerling-Leffler, J. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev. Neurobiol. 71, 45–61 (2011).

    PubMed  PubMed Central  Google Scholar 

  58. Lee, S., Hjerling-Leffler, J., Zagha, E., Fishell, G. & Rudy, B. The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J. Neurosci. 30, 16796–16808 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Varga, V. et al. Fast synaptic subcortical control of hippocampal circuits. Science 326, 449–453 (2009).

    CAS  PubMed  Google Scholar 

  60. Wozny, C. & Williams, S. R. Specificity of synaptic connectivity between layer 1 inhibitory interneurons and layer 2/3 pyramidal neurons in the rat neocortex. Cereb. Cortex 21, 1818–1826 (2011).

    PubMed  PubMed Central  Google Scholar 

  61. Brombas, A., Fletcher, L. N. & Williams, S. R. Activity-dependent modulation of layer 1 inhibitory neocortical circuits by acetylcholine. J. Neurosci. 34, 1932–1941 (2014).

    CAS  PubMed  Google Scholar 

  62. Simon, A., Olah, S., Molnar, G., Szabadics, J. & Tamas, G. Gap-junctional coupling between neurogliaform cells and various interneuron types in the neocortex. J. Neurosci. 25, 6278–6285 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Zsiros, V. & Maccaferri, G. Electrical coupling between interneurons with different excitable properties in the stratum lacunosum-moleculare of the juvenile CA1 rat hippocampus. J. Neurosci. 25, 8686–8695 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Zsiros, V., Aradi, I. & Maccaferri, G. Propagation of postsynaptic currents and potentials via gap junctions in GABAergic networks of the rat hippocampus. J. Physiol. 578, 527–544 (2007).

    CAS  PubMed  Google Scholar 

  65. Banks, M. I., White, J. A. & Pearce, R. A. Interactions between distinct GABAA circuits in hippocampus. Neuron 25, 449–457 (2000).

    CAS  PubMed  Google Scholar 

  66. White, J. A., Banks, M. I., Pearce, R. A. & Kopell, N. J. Networks of interneurons with fast and slow γ-aminobutyric acid type A (GABAA) kinetics provide substrate for mixed gamma–theta rhythm. Proc. Natl Acad. Sci. USA 97, 8128–8133 (2000).

    CAS  PubMed  Google Scholar 

  67. Bartos, M., Vida, I. & Jonas, P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat. Rev. Neurosci. 8, 45–56 (2007).

    CAS  PubMed  Google Scholar 

  68. Pernia-Andrade, A. J. & Jonas, P. Theta–gamma-modulated synaptic currents in hippocampal granule cells in vivo define a mechanism for network oscillations. Neuron 81, 140–152 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Wulff, P. et al. Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons. Proc. Natl Acad. Sci. USA 106, 3561–3566 (2009).

    CAS  PubMed  Google Scholar 

  70. Cutsuridis, V. & Hasselmo, M. GABAergic contributions to gating, timing, and phase precession of hippocampal neuronal activity during theta oscillations. Hippocampus 22, 1597–1621 (2012).

    CAS  PubMed  Google Scholar 

  71. Lapray, D. et al. Behavior-dependent specialization of identified hippocampal interneurons. Nat. Neurosci. 15, 1265–1271 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Ewell, L. A. & Jones, M. V. Frequency-tuned distribution of inhibition in the dentate gyrus. J. Neurosci. 30, 12597–12607 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Sambandan, S., Sauer, J. F., Vida, I. & Bartos, M. Associative plasticity at excitatory synapses facilitates recruitment of fast-spiking interneurons in the dentate gyrus. J. Neurosci. 30, 11826–11837 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. 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).

    CAS  PubMed  Google Scholar 

  75. Dieni, C. V., Chancey, J. H. & Overstreet-Wadiche, L. S. Dynamic functions of GABA signaling during granule cell maturation. Front. Neural Circuits 6, 113 (2012).

    PubMed  Google Scholar 

  76. Ge, S. et al. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439, 589–593 (2006).

    CAS  PubMed  Google Scholar 

  77. Jagasia, R. et al. GABA–cAMP response element-binding protein signaling regulates maturation and survival of newly generated neurons in the adult hippocampus. J. Neurosci. 29, 7966–7977 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Esposito, M. S. et al. Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J. Neurosci. 25, 10074–10086 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Overstreet Wadiche, L., Bromberg, D. A., Bensen, A. L. & Westbrook, G. L. GABAergic signaling to newborn neurons in dentate gyrus. J. Neurophysiol. 94, 4528–4532 (2005).

    PubMed  Google Scholar 

  80. Markwardt, S. J., Wadiche, J. I. & Overstreet-Wadiche, L. S. Input-specific GABAergic signaling to newborn neurons in adult dentate gyrus. J. Neurosci. 29, 15063–15072 (2009). This study shows that GABA A receptor-mediated synaptic signaling to adult-born neurons has characteristics of spillover-mediated transmission.

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Gaiarsa, J. L. & Porcher, C. Emerging neurotrophic role of GABAB receptors in neuronal circuit development. Front. Cell Neurosci. 7, 206 (2013).

    PubMed  PubMed Central  Google Scholar 

  82. Overstreet, L. S. & Westbrook, G. L. Synapse density regulates independence at unitary inhibitory synapses. J. Neurosci. 23, 2618–2626 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Song, J. et al. Parvalbumin interneurons mediate neuronal circuitry–neurogenesis coupling in the adult hippocampus. Nat. Neurosci. 16, 1728–1730 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Chancey, J. H. et al. GABA depolarization is required for experience-dependent synapse unsilencing in adult-born neurons. J. Neurosci. 33, 6614–6622 (2013). This study shows that slow synaptic GABA signalling to adult born neurons provides depolarization needed for AMPA-receptor incorporation at silent synapses.

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Chancey, J. H., Poulsen, D. J., Wadiche, J. I. & Overstreet-Wadiche, L. Hilar mossy cells provide the first glutamatergic synapses to adult-born dentate granule cells. J. Neurosci. 34, 2349–2354 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Wonders, C. P. & Anderson, S. A. The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 7, 687–696 (2006).

    CAS  PubMed  Google Scholar 

  87. Batista-Brito, R. & Fishell, G. The developmental integration of cortical interneurons into a functional network. Curr. Top. Dev. Biol. 87, 81–118 (2009).

    PubMed  PubMed Central  Google Scholar 

  88. Gelman, D. M. & Marin, O. Generation of interneuron diversity in the mouse cerebral cortex. Eur. J. Neurosci. 31, 2136–2141 (2010).

    PubMed  Google Scholar 

  89. Chittajallu, R. et al. Dual origins of functionally distinct O-LM interneurons revealed by differential 5-HT3AR expression. Nat. Neurosci. 16, 1598–1607 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Kepecs, A. & Fishell, G. Interneuron cell types are fit to function. Nature 505, 318–326 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Tricoire, L. & Vitalis, T. Neuronal nitric oxide synthase expressing neurons: a journey from birth to neuronal circuits. Front. Neural Circuits 6, 82 (2012).

    PubMed  PubMed Central  Google Scholar 

  92. Rancillac, A. et al. Glutamatergic control of microvascular tone by distinct GABA neurons in the cerebellum. J. Neurosci. 26, 6997–7006 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Craig, M. T. & McBain, C. J. Navigating the circuitry of the brain's GPS system: future challenges for neurophysiologists. Hippocampus http://dx.doi.org/10.1002/hipo.22456 (2015).

Download references

Author information

Authors and Affiliations

  1. Department of Neurobiology, McKnight Brain Institute, University of Alabama at Birmingham, Shelby Building 1003, 1825 University Boulevard, Birmingham, 35294, Alabama, USA

    Linda Overstreet-Wadiche

  2. Program in Developmental Neurobiology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Porter Neuroscience, Building 35, Room 3C903, Lincoln Drive, Bethesda, 20892, Maryland, USA

    Chris J. McBain

Authors
  1. Linda Overstreet-Wadiche
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chris J. McBain
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chris J. McBain.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

PowerPoint slides

Glossary

Subfield

Divisions within the hippocampus largely based on anatomical or cellular properties.

Stratum radiatum

A region of the hippocampus representing the primary termination zone of the Schaffer collateral axons of CA3 pyramidal cells.

Stratum lacunosum moleculare

A region of the hippocampus that primary receives inputs from the entorhinal cortex and thalamus as well as other subcortical afferents.

Arborization

The tree-like termination pattern of a neuronal axon.

Slow integration

The processing of excitatory (or inhibitory) inputs onto a cell across a time domain of seconds to minutes.

Temporoammonic pathway

An afferent projection primarily arising from pyramidal cells of the layer III entorhinal cortex and terminating in the CA1, CA2 and subiculum of the hippocampus.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Overstreet-Wadiche, L., McBain, C. Neurogliaform cells in cortical circuits. Nat Rev Neurosci 16, 458–468 (2015). https://doi.org/10.1038/nrn3969

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrn3969

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing