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

Nature Neuroscience volume 8, pages 15521559 (2005) | Download Citation

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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.

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References

  1. 1.

    & Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47 (1991).

  2. 2.

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

  3. 3.

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

  4. 4.

    , & A morphological basis for orientation tuning in primary visual cortex. Nat. Neurosci. 7, 872–879 (2004).

  5. 5.

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

  6. 6.

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

  7. 7.

    & Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex. J. Neurosci. 9, 2432–2442 (1989).

  8. 8.

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

  9. 9.

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

  10. 10.

    , & Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402, 75–79 (1999).

  11. 11.

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

  12. 12.

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

  13. 13.

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

  14. 14.

    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).

  15. 15.

    , & Two functional channels from primary visual cortex to dorsal visual cortical areas. Science 292, 297–300 (2001).

  16. 16.

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

  17. 17.

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

  18. 18.

    & Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons. Nat. Neurosci. 3, 701–707 (2000).

  19. 19.

    , , , & Geometric and functional organization of cortical circuits. Nat. Neurosci (2005).

  20. 20.

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

  21. 21.

    , , , & Cell type-specific circuits of cortical layer IV spiny neurons. J. Neurosci. 23, 2961–2970 (2003).

  22. 22.

    , , , & Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol. 3, e68 (2005).

  23. 23.

    , & Excitatory cortical neurons form fine-scale functional networks. Nature 433, 868–873 (2005).

  24. 24.

    , , & Dynamics of neuronal firing correlation: modulation of 'effective connectivity'. J. Neurophysiol. 61, 900–917 (1989).

  25. 25.

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

  26. 26.

    & Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci. 13, 99–104 (1990).

  27. 27.

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

  28. 28.

    , & Molecular diversity of neocortical GABAergic interneurones. J. Physiol. (Lond.) 562, 99–105 (2005).

  29. 29.

    , , & Pyramidal cell communication within local networks in layer 2/3 of rat neocortex. J. Physiol. (Lond.) 551, 139–153 (2003).

  30. 30.

    & Synaptic activity and the construction of cortical circuits. Science 274, 1133–1138 (1996).

  31. 31.

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

  32. 32.

    , , , & Recurrent excitation in neocortical circuits. Science 269, 981–985 (1995).

  33. 33.

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

  34. 34.

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

  35. 35.

    & Different roles for simple-cell and complex-cell inhibition in V1. J. Neurosci. 23, 10201–10213 (2003).

  36. 36.

    , , & Salient features of synaptic organisation in the cerebral cortex. Brain Res. Brain Res. Rev. 26, 113–135 (1998).

  37. 37.

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

  38. 38.

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

  39. 39.

    , , & Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat. Neurosci. 3, 366–371 (2000).

  40. 40.

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

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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

Affiliations

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

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Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Edward M Callaway.

Supplementary information

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  1. 1.

    Supplementary Fig. 1

    Organization of cortical connections revealed by this study and incorporating data from a previous study.

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DOI

https://doi.org/10.1038/nn1565

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