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.

  • Article
  • Published:

Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons

Abstract

The functional role of an individual neuron within a cortical circuit is largely determined by that neuron's synaptic input. We examined the laminar sources of local input to subtypes of cortical neurons in layer 2/3 of rat visual cortex using laser scanning photostimulation. We identified three distinct laminar patterns of excitatory input that correspond to physiological and morphological subtypes of neurons. Fast-spiking inhibitory basket cells and excitatory pyramidal neurons received strong excitatory input from middle cortical layers. In contrast, adapting inhibitory interneurons received their strongest excitatory input either from deep layers or laterally from within layer 2/3. Thus, differential laminar sources of excitatory inputs contribute to the functional diversity of cortical inhibitory interneurons.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Spatial resolution of laser-scanning photostimulation.
Figure 2: Laminar excitatory input to layer 2/3 cortical neurons falls into three patterns.
Figure 4: Laminar excitatory input is homogeneous to fast-spiking interneurons, but adapting interneurons fall into two groups.
Figure 3: Types of layer 2/3 interneurons and pyramidal neurons for which laminar synaptic input was mapped in rat visual cortex.
Figure 5: Laminar patterns of excitatory input are not due to differential inhibitory input.

Similar content being viewed by others

References

  1. Peters, A. & Regidor, J. A reassessment of the forms of nonpyramidal neurons in area 17 of cat visual cortex. J. Comp. Neurol. 203, 685–716 (1981).

    CAS  PubMed  Google Scholar 

  2. Parra, P., Gulyas, A. I. & Miles, R. How many subtypes of inhibitory cells in the hippocampus? Neuron 20, 983–993 (1998).

    CAS  PubMed  Google Scholar 

  3. Thomson, A. M. & Deuchars, J. Synaptic interactions in neocortical local circuits: dual intracellular recordings in vitro. Cereb. Cortex 7, 510–522 (1997).

    CAS  PubMed  Google Scholar 

  4. Kawaguchi, Y. Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J. Neurophysiol. 69, 416–431 (1993).

    CAS  PubMed  Google Scholar 

  5. Cauli, B. et al. Molecular and physiological diversity of cortical nonpyramidal cells. J. Neurosci. 17, 3894–3906 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Gonchar, Y. & Burkhalter, A. Three distinct families of GABAergic neurons in rat visual cortex. Cereb. Cortex 7, 347–358 (1997).

    CAS  PubMed  Google Scholar 

  7. Gupta, A., Wang, Y. & Markram, H. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287, 273–278 (2000).

    CAS  PubMed  Google Scholar 

  8. Somogyi, P., Tamas, G., Lujan, R. & Buhl, E. H. Salient features of synaptic organisation in the cerebral cortex. Brain Res. Rev. 26, 113–135 (1998).

    CAS  PubMed  Google Scholar 

  9. Rockland, K. S. Complex microstructures of sensory cortical connections. Curr. Opin. Neurobiol. 8, 545–551 (1998).

    CAS  PubMed  Google Scholar 

  10. Gilbert, C. D. Microcircuitry of the visual cortex. Annu. Rev. Neurosci. 6, 217–247 (1983).

    CAS  PubMed  Google Scholar 

  11. Callaway, E. M. Local circuits in primary visual cortex of the macaque monkey. Annu. Rev. Neurosci. 21, 47–74 (1998).

    CAS  PubMed  Google Scholar 

  12. Ahmed, B., Anderson, J. C., Martin, K. A. & Nelson, J. C. Map of the synapses onto layer 4 basket cells of the primary visual cortex of the cat. J. Comp. Neurol. 380, 230–242 (1997).

    CAS  PubMed  Google Scholar 

  13. Anderson, J. C., Douglas, R. J., Martin, K. A. C. & Nelson, J. C. Map of the synapses formed with the dendrites of spiny stellate neurons of cat visual cortex. J. Comp. Neurol. 341, 25–38 (1994).

    CAS  PubMed  Google Scholar 

  14. Hornung, J. P. & Celio, M. R. The selective innervation by serotonergic axons of calbindin-containing interneurons in the neocortex and hippocampus of the marmoset. J. Comp. Neurol. 320, 457–467 (1992).

    CAS  PubMed  Google Scholar 

  15. Freund, T. F. & Gulyas, A. I. GABAergic interneurons containing calbindin D28K or somatostatin are major targets of GABAergic basal forebrain afferents in the rat neocortex. J. Comp. Neurol. 314, 187–199 (1991).

    CAS  PubMed  Google Scholar 

  16. Staiger, J. F., Zilles, K. & Freund, T. F. Distribution of GABAergic elements postsynaptic to ventroposteromedial thalamic projections in layer IV of rat barrel cortex. Eur. J. Neurosci. 8, 2273–2285 (1996).

    CAS  PubMed  Google Scholar 

  17. Gibson, J. R., Beierlein, M. & Connors, B. W. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402, 75–79 (1999).

    CAS  PubMed  Google Scholar 

  18. Somogyi, P. A specific ‘axo-axonal’ interneuron in the visual cortex of the rat. Brain Res. 136, 345–350 (1977).

    CAS  PubMed  Google Scholar 

  19. Somogyi, P., Kisvarday, Z. F., Martin, K. A. & Whitteridge, D. Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat. Neuroscience 10, 261–294 (1983).

    CAS  PubMed  Google Scholar 

  20. Meskenaite, V. Calretinin-immunoreactive local circuit neurons in area 17 of the cynomolgus monkey, Macaca fascicularis. J. Comp. Neurol. 379, 113–132 (1997).

    CAS  PubMed  Google Scholar 

  21. Gonchar, Y. & Burkhalter, A. Connectivity of GABAergic calretinin-immunoreactive neurons in rat primary visual cortex. Cereb. Cortex 9, 683–696 (1999).

    CAS  PubMed  Google Scholar 

  22. Defelipe, J., Gonzalez-Albo, M. C., Del Rio, M. R. & Elston, G. N. Distribution and patterns of connectivity of interneurons containing calbindin, calretinin, and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey. J. Comp. Neurol. 412, 515–526 (1999).

    CAS  PubMed  Google Scholar 

  23. Tamas, G., Somogyi, P. & Buhl, E. H. Differentially interconnected networks of GABAergic interneurons in the visual cortex of the cat. J. Neurosci. 18, 4255–4270 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Katz, L. C. & Dalva, M. B. Scanning laser photostimulation: a new approach for analyzing brain circuits. J. Neurosci. Methods 54, 205–218 (1994).

    CAS  PubMed  Google Scholar 

  25. Callaway, E. M. & Katz, L. C. Photostimulation using caged glutamate reveals functional circuitry in living brain slices. Proc. Natl. Acad. Sci. USA 90, 7661–7665 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Parnavelas, J. G. Development of GABA-containing neurons in the visual cortex. Prog. Brain Res. 90, 523–537 (1992).

    CAS  PubMed  Google Scholar 

  27. Thomson, A. M. & Bannister, A. P. Postsynaptic pyramidal target selection by descending layer III pyramidal axons: dual intracellular recordings and biocytin filling in slices of rat neocortex. Neuroscience 84, 669–683 (1998).

    CAS  PubMed  Google Scholar 

  28. Stevens, C. F. & Wang, Y. Facilitation and depression at single central synapses. Neuron 14, 795–802 (1995).

    CAS  PubMed  Google Scholar 

  29. Kawaguchi, Y. & Kubota, Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7, 476–486 (1997).

    CAS  PubMed  Google Scholar 

  30. McCormick, D. A., Connors, B. W., Lighthall, J. W. & Prince, D. A. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J. Neurophysiol. 54, 782–806 (1985).

    CAS  PubMed  Google Scholar 

  31. Connors, B. W. & Gutnick, M. J. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci. 13, 99–104 (1990).

    CAS  PubMed  Google Scholar 

  32. Jones, E. G. & Hendry, S. H. C. in Cerebral Cortex (eds. Peters, A. & Jones, E. G.) 309–336 (Plenum, New York, 1984).

    Google Scholar 

  33. Kawaguchi, Y. & Kubota, Y. Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neuroscience 85, 677–701 (1998).

    CAS  PubMed  Google Scholar 

  34. 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  PubMed Central  Google Scholar 

  35. Zhang, Z. W. & Deschenes, M. Intracortical axonal projections of lamina VI cells of the primary somatosensory cortex in the rat: a single-cell labeling study. J. Neurosci. 17, 6365–6379 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Burkhalter, A. Intrinsic connections of rat primary visual cortex: laminar organization of axonal projections. J. Comp. Neurol. 279, 171–186 (1989).

    CAS  PubMed  Google Scholar 

  37. Larkum, M. E., Zhu, J. J. & Sakmann, B. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398, 338–341 (1999).

    CAS  PubMed  Google Scholar 

  38. Kim, H. G., Beierlein, M. & Connors, B. W. Inhibitory control of excitable dendrites in neocortex. J. Neurophysiol. 74, 1810–1814 (1995).

    CAS  PubMed  Google Scholar 

  39. Tarczy-Hornoch, K., Martin, K. A., Stratford, K. J. & Jack, J. J. Intracortical excitation of spiny neurons in layer 4 of cat striate cortex in vitro. Cereb. Cortex 9, 833–843 (1999).

    CAS  PubMed  Google Scholar 

  40. Braitenberg, V. & Schuz, A. Anatomy of the Cortex (Springer, Berlin, 1991).

    Google Scholar 

  41. Reyes, A. & Sakmann, B. Developmental switch in the short term modification of unitary EPSPs evoked in layer 2/3 and layer 5 pyramidal neurons of rat neocortex. J. Neurosci. 19, 3827–3835 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Felleman, D. J. & Van Essen, D. C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47 (1991).

    CAS  PubMed  Google Scholar 

  43. Kisvarday, Z. F., Martin, K. A., Whitteridge, D. & Somogyi, P. Synaptic connections of intracellularly filled clutch cells: a type of small basket cell in the visual cortex of the cat. J. Comp. Neurol. 241, 111–137 (1985).

    CAS  PubMed  Google Scholar 

  44. Freund, T. F., Magloczky, Z., Soltesz, I. & Somogyi, P. Synaptic connections, axonal and dendritic patterns of neurons immunoreactive for cholecystokinin in the visual cortex of the cat. Neuroscience 19, 1133–1159 (1986).

    CAS  PubMed  Google Scholar 

  45. Reyes, A. et al. Target-cell-specific facilitation and depression in neocortical circuits. Nat. Neurosci. 1, 279–285 (1998).

    CAS  PubMed  Google Scholar 

  46. Galarreta, M. & Hestrin, S. Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nat. Neurosci. 1, 587–594 (1998).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by an NIH grant (E.M.C.) and an NSF graduate research fellowship, NIH training grants and the Chapman Charitable Trust (J.L.D). We thank A. Sawatari for discussions and technical assistance, A. Burkhalter, M. Dantzker, N. Spitzer, C. Stevens, and members of the lab for comments on the manuscript, and E. Huang for providing peak analysis software.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. L. Dantzker.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dantzker, J., Callaway, E. Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons. Nat Neurosci 3, 701–707 (2000). https://doi.org/10.1038/76656

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/76656

This article is cited by

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