Three Types of Cortical Layer 5 Neurons That Differ in Brain-wide Connectivity and Function

Neuron

Volumn 88, Issue 6, 2015, Pages 1253-1267

  Kim, Euiseok J ^a   Juavinett, Ashley L ^a,b   Kyubwa, Espoir M ^a,b   Jacobs, Matthew W ^a   Callaway, Edward M ^a,b  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; ASSOCIATION CORTEX; BRAIN CELL; CINGULATE GYRUS; CONTROLLED STUDY; CORTEX LAYER V; CORTICOCORTICAL NEURON; CORTICOSUBCORTICAL NEURON; FOREBRAIN; MOUSE; NERVE CELL NETWORK; NERVE PROJECTION; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RETROSPLENIAL CORTEX; STRIATE CORTEX; THALAMUS; VISUAL INFORMATION; ANIMAL; C57BL MOUSE; CYTOLOGY; NERVE CELL; PHYSIOLOGY; TRANSGENIC MOUSE; VISUAL CORTEX;

ANIMALS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE NET; NEURONS; PYRAMIDAL CELLS; VISUAL CORTEX;

EID: 84961653942     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.11.002     Document Type: Article

References (54)

1. Adesnik H., Bruns W., Taniguchi H., Huang Z.J., Scanziani M. A neural circuit for spatial summation in visual cortex. Nature 2012, 490:226-231.
2. Andermann M.L., Kerlin A.M., Roumis D.K., Glickfeld L.L., Reid R.C. Functional specialization of mouse higher visual cortical areas. Neuron 2011, 72:1025-1039.
3. Bortone D.S., Olsen S.R., Scanziani M. Translaminar inhibitory cells recruited by layer 6 corticothalamic neurons suppress visual cortex. Neuron 2014, 82:474-485.
4. Bourassa J., Deschênes M. Corticothalamic projections from the primary visual cortex in rats: a single fiber study using biocytin as an anterograde tracer. Neuroscience 1995, 66:253-263.
5. Constantinople C.M., Bruno R.M. Deep cortical layers are activated directly by thalamus. Science 2013, 340:1591-1594.
6. Cowan R.L., Wilson C.J. Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. J. Neurophysiol. 1994, 71:17-32.
7. Day M., Carr D.B., Ulrich S., Ilijic E., Tkatch T., Surmeier D.J. Dendritic excitability of mouse frontal cortex pyramidal neurons is shaped by the interaction among HCN, Kir2, and Kleak channels. J. Neurosci. 2005, 25:8776-8787.
8. Douglas R.J., Martin K.A.C. Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 2004, 27:419-451.
9. Ferster D., Lindström S. An intracellular analysis of geniculo-cortical connectivity in area 17 of the cat. J. Physiol. 1983, 342:181-215.
10. Finlay B.L., Schiller P.H., Volman S.F. Quantitative studies of single-cell properties in monkey striate cortex. IV. Corticotectal cells. J. Neurophysiol. 1976, 39:1352-1361.
11. Fu Y., Tucciarone J.M., Espinosa J.S., Sheng N., Darcy D.P., Nicoll R.A., Huang Z.J., Stryker M.P. A cortical circuit for gain control by behavioral state. Cell 2014, 156:1139-1152.
12. Garrett M.E., Nauhaus I., Marshel J.H., Callaway E.M. Topography and areal organization of mouse visual cortex. J. Neurosci. 2014, 34:12587-12600.
13. Gerfen C.R., Paletzki R., Heintz N. GENSAT BAC cre-recombinase driver lines to study the functional organization of cerebral cortical and basal ganglia circuits. Neuron 2013, 80:1368-1383.
14. Gong S., Doughty M., Harbaugh C.R., Cummins A., Hatten M.E., Heintz N., Gerfen C.R. Targeting Cre recombinase to specific neuron populations with bacterial artificial chromosome constructs. J. Neurosci. 2007, 27:9817-9823.
15. Groh A., Meyer H.S., Schmidt E.F., Heintz N., Sakmann B., Krieger P. Cell-type specific properties of pyramidal neurons in neocortex underlying a layout that is modifiable depending on the cortical area. Cereb. Cortex 2010, 20:826-836.
16. Grubb M.S., Thompson I.D. Quantitative characterization of visual response properties in the mouse dorsal lateral geniculate nucleus. J. Neurophysiol. 2003, 90:3594-3607.
17. 2+ dependence and differential modulation by norepinephrine. J. Neurophysiol. 2015, 113:2014-2032.
18. Hallman L.E., Schofield B.R., Lin C.S. Dendritic morphology and axon collaterals of corticotectal, corticopontine, and callosal neurons in layer V of primary visual cortex of the hooded rat. J. Comp. Neurol. 1988, 272:149-160.
19. Hattox A.M., Nelson S.B. Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. J. Neurophysiol. 2007, 98:3330-3340.
20. Hübener M., Bolz J. Morphology of identified projection neurons in layer 5 of rat visual cortex. Neurosci. Lett. 1988, 94:76-81.
21. Hübener M., Schwarz C., Bolz J. Morphological types of projection neurons in layer 5 of cat visual cortex. J. Comp. Neurol. 1990, 301:655-674.
22. Kasper E.M., Larkman A.U., Lübke J., Blakemore C. Pyramidal neurons in layer 5 of the rat visual cortex. I. Correlation among cell morphology, intrinsic electrophysiological properties, and axon targets. J. Comp. Neurol. 1994, 339:459-474.
23. Kim J., Matney C.J., Blankenship A., Hestrin S., Brown S.P. Layer 6 corticothalamic neurons activate a cortical output layer, layer 5a. J. Neurosci. 2014, 34:9656-9664.
24. Krauzlis R.J., Lovejoy L.P., Zénon A. Superior colliculus and visual spatial attention. Annu. Rev. Neurosci. 2013, 36:165-182.
25. Larkman A.U., Mason A., Blakemore C. The in vitro slice preparation for combined morphological and electrophysiological studies of rat visual cortex. Neurosci. Res. 1988, 6:1-19.
26. Larsen D.D., Wickersham I.R., Callaway E.M. Retrograde tracing with recombinant rabies virus reveals correlations between projection targets and dendritic architecture in layer 5 of mouse barrel cortex. Front. Neural Circuits 2007, 1:5.
27. Lee S.H., Kwan A.C., Zhang S., Phoumthipphavong V., Flannery J.G., Masmanidis S.C., Taniguchi H., Huang Z.J., Zhang F., Boyden E.S., et al. Activation of specific interneurons improves V1 feature selectivity and visual perception. Nature 2012, 488:379-383.
28. Lee S., Kruglikov I., Huang Z.J., Fishell G., Rudy B. A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nat. Neurosci. 2013, 16:1662-1670.
29. Levesque M., Charara A., Gagnon S., Parent A., Deschenes M. Corticostriatal projections from layer V cells in rat are collaterals of long-range corticofugal axons. Brain Res. 1996, 709:311-315.
30. Li J., Wang S., Bickford M.E. Comparison of the ultrastructure of cortical and retinal terminals in the rat dorsal lateral geniculate and lateral posterior nuclei. J. Comp. Neurol. 2003, 460:394-409.
31. Li N., Chen T.W., Guo Z.V., Gerfen C.R., Svoboda K. A motor cortex circuit for motor planning and movement. Nature 2015, 519:51-56.
32. Madisen L., Mao T., Koch H., Zhuo J.M., Berenyi A., Fujisawa S., Hsu Y.W., Garcia A.J., Gu X., Zanella S., et al. A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat. Neurosci. 2012, 15:793-802.
33. Marshel J.H., Garrett M.E., Nauhaus I., Callaway E.M. Functional specialization of seven mouse visual cortical areas. Neuron 2011, 72:1040-1054.
34. Miyamichi K., Shlomai-Fuchs Y., Shu M., Weissbourd B.C., Luo L., Mizrahi A. Dissecting local circuits: parvalbumin interneurons underlie broad feedback control of olfactory bulb output. Neuron 2013, 80:1232-1245.
35. Molyneaux B.J., Arlotta P., Menezes J.R.L., Macklis J.D. Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 2007, 8:427-437.
36. Niell C.M., Stryker M.P. Highly selective receptive fields in mouse visual cortex. J. Neurosci. 2008, 28:7520-7536.
37. Niell C.M., Stryker M.P. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 2010, 65:472-479.
38. Nienborg H., Hasenstaub A., Nauhaus I., Taniguchi H., Huang Z.J., Callaway E.M. Contrast dependence and differential contributions from somatostatin- and parvalbumin-expressing neurons to spatial integration in mouse V1. J. Neurosci. 2013, 33:11145-11154.
39. O'Leary D.D., Koester S.E. Development of projection neuron types, axon pathways, and patterned connections of the mammalian cortex. Neuron 1993, 10:991-1006.
40. Olsen S.R., Bortone D.S., Adesnik H., Scanziani M. Gain control by layer six in cortical circuits of vision. Nature 2012, 483:47-52.
41. Palmer L.A., Rosenquist A.C. Visual receptive fields of single striate corical units projecting to the superior colliculus in the cat. Brain Res. 1974, 67:27-42.
42. Paxinos G., Franklin K.B.J., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates 2001, Academic Press, San Diego. Second Edition.
43. Schubert D., Staiger J.F., Cho N., Kötter R., Zilles K., Luhmann H.J. Layer-specific intracolumnar and transcolumnar functional connectivity of layer V pyramidal cells in rat barrel cortex. J. Neurosci. 2001, 21:3580-3592.
44. Sheets P.L., Suter B.A., Kiritani T., Chan C.S., Surmeier D.J., Shepherd G.M. Corticospinal-specific HCN expression in mouse motor cortex: I(h)-dependent synaptic integration as a candidate microcircuit mechanism involved in motor control. J. Neurophysiol. 2011, 106:2216-2231.
45. Sorensen S.A., Bernard A., Menon V., Royall J.J., Glattfelder K.J., Desta T., Hirokawa K., Mortrud M., Miller J.A., Zeng H., et al. Correlated gene expression and target specificity demonstrate excitatory projection neuron diversity. Cereb. Cortex 2013, 25:443-449.
46. Taniguchi H., He M., Wu P., Kim S., Paik R., Sugino K., Kvitsiani D., Fu Y., Lu J., Lin Y., et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 2011, 71:995-1013.
47. Tsiola A., Hamzei-Sichani F., Peterlin Z., Yuste R. Quantitative morphologic classification of layer 5 neurons from mouse primary visual cortex. J. Comp. Neurol. 2003, 461:415-428.
48. Van Essen D.C. Corticocortical and thalamocortical information flow in the primate visual system. Prog. Brain Res. 2005, 149:173-185.
49. Vélez-Fort M., Rousseau C.V., Niedworok C.J., Wickersham I.R., Rancz E.A., Brown A.P.Y., Strom M., Margrie T.W. The stimulus selectivity and connectivity of layer six principal cells reveals cortical microcircuits underlying visual processing. Neuron 2014, 83:1431-1443.
50. Wall N.R., Wickersham I.R., Cetin A., De La Parra M., Callaway E.M. Monosynaptic circuit tracing in vivo through Cre-dependent targeting and complementation of modified rabies virus. Proc. Natl. Acad. Sci. USA 2010, 107:21848-21853.
51. Wickersham I.R., Lyon D.C., Barnard R.J.O., Mori T., Finke S., Conzelmann K.-K., Young J.A.T., Callaway E.M. Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron 2007, 53:639-647.
52. Wilson N.R., Runyan C.A., Wang F.L., Sur M. Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 2012, 488:343-348.
53. Zarrinpar A., Callaway E.M. Functional local input to layer 5 pyramidal neurons in the rat visual cortex. Cereb. Cortex 2014, 10.1093/cercor/bhu268.
54. Zhang S., Xu M., Kamigaki T., Hoang Do J.P., Chang W.C., Jenvay S., Miyamichi K., Luo L., Dan Y. Selective attention. Long-range and local circuits for top-down modulation of visual cortex processing. Science 2014, 345:660-665.