Article | Published:

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

Nature Neuroscience volume 3, pages 701707 (2000) | Download Citation

Subjects

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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

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

  2. 2.

    , & How many subtypes of inhibitory cells in the hippocampus? Neuron 20, 983–993 (1998).

  3. 3.

    & Synaptic interactions in neocortical local circuits: dual intracellular recordings in vitro. Cereb. Cortex 7, 510–522 (1997).

  4. 4.

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

  5. 5.

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

  6. 6.

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

  7. 7.

    , & Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287, 273–278 (2000).

  8. 8.

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

  9. 9.

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

  10. 10.

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

  11. 11.

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

  12. 12.

    , , & Map of the synapses onto layer 4 basket cells of the primary visual cortex of the cat. J. Comp. Neurol. 380, 230–242 (1997).

  13. 13.

    , , & Map of the synapses formed with the dendrites of spiny stellate neurons of cat visual cortex. J. Comp. Neurol. 341, 25–38 (1994).

  14. 14.

    & 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).

  15. 15.

    & 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).

  16. 16.

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

  17. 17.

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

  18. 18.

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

  19. 19.

    , , & Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat. Neuroscience 10, 261–294 (1983).

  20. 20.

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

  21. 21.

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

  22. 22.

    , , & 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).

  23. 23.

    , & Differentially interconnected networks of GABAergic interneurons in the visual cortex of the cat. J. Neurosci. 18, 4255–4270 (1998).

  24. 24.

    & Scanning laser photostimulation: a new approach for analyzing brain circuits. J. Neurosci. Methods 54, 205–218 (1994).

  25. 25.

    & Photostimulation using caged glutamate reveals functional circuitry in living brain slices. Proc. Natl. Acad. Sci. USA 90, 7661–7665 (1993).

  26. 26.

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

  27. 27.

    & 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).

  28. 28.

    & Facilitation and depression at single central synapses. Neuron 14, 795–802 (1995).

  29. 29.

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

  30. 30.

    , , & Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J. Neurophysiol. 54, 782–806 (1985).

  31. 31.

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

  32. 32.

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

  33. 33.

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

  34. 34.

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

  35. 35.

    & 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).

  36. 36.

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

  37. 37.

    , & A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398, 338–341 (1999).

  38. 38.

    , & Inhibitory control of excitable dendrites in neocortex. J. Neurophysiol. 74, 1810–1814 (1995).

  39. 39.

    , , & Intracortical excitation of spiny neurons in layer 4 of cat striate cortex in vitro. Cereb. Cortex 9, 833–843 (1999).

  40. 40.

    & Anatomy of the Cortex (Springer, Berlin, 1991).

  41. 41.

    & 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).

  42. 42.

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

  43. 43.

    , , & 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).

  44. 44.

    , , & Synaptic connections, axonal and dendritic patterns of neurons immunoreactive for cholecystokinin in the visual cortex of the cat. Neuroscience 19, 1133–1159 (1986).

  45. 45.

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

  46. 46.

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

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

Affiliations

  1. Systems Neurobiology Laboratories, The Salk Institute for Biological Studies, 10010 N. Torrey Pines Rd., La Jolla, California, 92037, USA, and Department of Biology, University of California San Diego, La Jolla, California, USA

    • J. L. Dantzker
    •  & E. M. Callaway

Authors

  1. Search for J. L. Dantzker in:

  2. Search for E. M. Callaway in:

Corresponding author

Correspondence to J. L. Dantzker.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/76656

Further reading