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.

Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity

Nature Neuroscience volume 8, pages 1552–1559 (2005)Cite this article

Abstract

Excitatory cortical neurons form fine-scale networks of precisely interconnected neurons. Here we tested whether inhibitory cortical neurons in rat visual cortex might also be connected with fine-scale specificity. Using paired intracellular recordings and cross-correlation analyses of photostimulation-evoked synaptic currents, we found that fast-spiking interneurons preferentially connected to neighboring pyramids that provided them with reciprocal excitation. Furthermore, they shared common fine-scale excitatory input with neighboring pyramidal neurons only when the two cells were reciprocally connected, and not when there was no connection or a one-way, inhibitory-to-excitatory connection. Adapting inhibitory neurons shared little or no common input with neighboring pyramids, regardless of their direct connectivity. We conclude that inhibitory connections and also excitatory connections to inhibitory neurons can both be precise on a fine scale. Furthermore, fine-scale specificity depends on the type of inhibitory neuron and on direct connectivity between neighboring pyramidal-inhibitory neuron pairs.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

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

Figure 1: Direct connections between layer 2/3 inhibitory neuron–pyramidal neuron pairs.
Figure 2: Cross-correlation analyses of photostimulation-evoked EPSCs simultaneously recorded in adjacent layer 2/3 neuron pairs consisting of one pyramidal neuron and one fast-spiking inhibitory neuron (FS).
Figure 3: Correlation probabilities for EPSCs measured simultaneously in fast-spiking interneuron–pyramidal neuron pairs.
Figure 4: Cross-correlation analyses of photostimulation-evoked EPSCs simultaneously recorded in adjacent layer 2/3 neuron pairs consisting of one pyramidal neuron and one adapting inhibitory neuron (AD).
Figure 5: Correlation probabilities for EPSCs measured simultaneously in adapting interneuron–pyramidal neuron pairs.

References

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

    Article  CAS  Google Scholar 

  2. Fitzpatrick, D. The functional organization of local circuits in visual cortex: insights from the study of tree shrew striate cortex. Cereb. Cortex 6, 329–341 (1996).

    Article  CAS  Google Scholar 

  3. Martin, K.A.C. in Cerebral Cortex, Vol. 2. (eds. Jones, E.G. & Peters, A.) 241–284 (Plenum, New York, 1984).

    Book  Google Scholar 

  4. Mooser, F., Bosking, W.H. & Fitzpatrick, D. A morphological basis for orientation tuning in primary visual cortex. Nat. Neurosci. 7, 872–879 (2004).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. Gilbert, C.D. & Wiesel, T.N. Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex. J. Neurosci. 9, 2432–2442 (1989).

    Article  CAS  Google Scholar 

  8. Lund, J.S. Anatomical organization of macaque monkey striate visual cortex. Annu. Rev. Neurosci. 11, 253–288 (1988).

    Article  CAS  Google Scholar 

  9. Agmon, A. & Connors, B.W. Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex. J. Neurosci. 12, 319–329 (1992).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  12. Gonchar, Y. & Burkhalter, A. Distinct GABAergic targets of feedforward and feedback connections between lower and higher areas of rat visual cortex. J. Neurosci. 23, 10904–10912 (2003).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  14. Staiger, J.F. et al. Innervation of interneurons immunoreactive for VIP by intrinsically bursting pyramidal cells and fast-spiking interneurons in infragranular layers of juvenile rat neocortex. Eur. J. Neurosci. 16, 11–20 (2002).

    Article  Google Scholar 

  15. Yabuta, N.H., Sawatari, A. & Callaway, E.M. Two functional channels from primary visual cortex to dorsal visual cortical areas. Science 292, 297–300 (2001).

    Article  CAS  Google Scholar 

  16. Sawatari, A. & Callaway, E.M. Diversity and cell type specificity of local excitatory connections to neurons in layer 3B of monkey primary visual cortex. Neuron 25, 459–471 (2000).

    Article  CAS  Google Scholar 

  17. Briggs, F. & Callaway, E.M. Layer-specific input to distinct cell types in layer 6 of monkey primary visual cortex. J. Neurosci. 21, 3600–3608 (2001).

    Article  CAS  Google Scholar 

  18. Dantzker, J.L. & Callaway, E.M. Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons. Nat. Neurosci. 3, 701–707 (2000).

    Article  CAS  Google Scholar 

  19. Shepherd, G.M., Stepanyants, A., Bureau, I., Chklovskii, D. & Svoboda, K. Geometric and functional organization of cortical circuits. Nat. Neurosci (2005).

  20. Schubert, D. et al. Layer-specific intracolumnar and transcolumnar functional connectivity of layer V pyramidal cells in rat barrel cortex. J. Neurosci. 21, 3580–3592 (2001).

    Article  CAS  Google Scholar 

  21. Schubert, D., Kotter, R., Zilles, K., Luhmann, H.J. & Staiger, J.F. Cell type-specific circuits of cortical layer IV spiny neurons. J. Neurosci. 23, 2961–2970 (2003).

    Article  CAS  Google Scholar 

  22. Song, S., Sjostrom, P.J., Reigl, M., Nelson, S. & Chklovskii, D.B. Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol. 3, e68 (2005).

    Article  Google Scholar 

  23. Yoshimura, Y., Dantzker, J.L. & Callaway, E.M. Excitatory cortical neurons form fine-scale functional networks. Nature 433, 868–873 (2005).

    Article  CAS  Google Scholar 

  24. Aertsen, A.M., Gerstein, G.L., Habib, M.K. & Palm, G. Dynamics of neuronal firing correlation: modulation of 'effective connectivity'. J. Neurophysiol. 61, 900–917 (1989).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  27. Kawaguchi, Y. & Kondo, S. Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex. J. Neurocytol. 31, 277–287 (2002).

    Article  Google Scholar 

  28. Blatow, M., Caputi, A. & Monyer, H. Molecular diversity of neocortical GABAergic interneurones. J. Physiol. (Lond.) 562, 99–105 (2005).

    Article  CAS  Google Scholar 

  29. Holmgren, C., Harkany, T., Svennenfors, B. & Zilberter, Y. Pyramidal cell communication within local networks in layer 2/3 of rat neocortex. J. Physiol. (Lond.) 551, 139–153 (2003).

    Article  CAS  Google Scholar 

  30. Katz, L.C. & Shatz, C.J. Synaptic activity and the construction of cortical circuits. Science 274, 1133–1138 (1996).

    Article  CAS  Google Scholar 

  31. Martin, K.A. Microcircuits in visual cortex. Curr. Opin. Neurobiol. 12, 418–425 (2002).

    Article  CAS  Google Scholar 

  32. Douglas, R.J., Koch, C., Mahowald, M., Martin, K.A. & Suarez, H.H. Recurrent excitation in neocortical circuits. Science 269, 981–985 (1995).

    Article  CAS  Google Scholar 

  33. Dragoi, V. & Sur, M. Dynamic properties of recurrent inhibition in primary visual cortex: contrast and orientation dependence of contextual effects. J. Neurophysiol. 83, 1019–1030 (2000).

    Article  CAS  Google Scholar 

  34. Swadlow, H.A. Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. Cereb. Cortex 13, 25–32 (2003).

    Article  Google Scholar 

  35. Lauritzen, T.Z. & Miller, K.D. Different roles for simple-cell and complex-cell inhibition in V1. J. Neurosci. 23, 10201–10213 (2003).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  37. Somogyi, P. & Klausberger, T. Defined types of cortical interneurone structure space and spike timing in the hippocampus. J. Physiol. (Lond.) 562, 9–26 (2005).

    Article  CAS  Google Scholar 

  38. Klausberger, T. et al. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421, 844–848 (2003).

    Article  CAS  Google Scholar 

  39. Tamas, G., Buhl, E.H., Lorincz, A. & Somogyi, P. Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat. Neurosci. 3, 366–371 (2000).

    Article  CAS  Google Scholar 

  40. Galarreta, M. & Hestrin, S. A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402, 72–75 (1999).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Supported by grants from the US National Institutes of Health (MH063912, EY010742) and from the Japanese Ministry of Education, Culture, Science, Sports and Technology (17023026, 17500208). We thank Y. Komatsu and H. Sato for discussions.

Author information

Authors and Affiliations

  1. Systems Neurobiology Laboratories, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, 92037, California, USA

    Yumiko Yoshimura & Edward M Callaway

  2. Department of Visual Neuroscience, Research Institute of Environmental Medicine, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8601, Japan

    Yumiko Yoshimura

Authors
  1. Yumiko Yoshimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Edward M Callaway
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Edward M Callaway.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Organization of cortical connections revealed by this study and incorporating data from a previous study. (PDF 580 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Yoshimura, Y., Callaway, E. Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity. Nat Neurosci 8, 1552–1559 (2005). https://doi.org/10.1038/nn1565

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1565

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