Motor cortex feedback influences sensory processing by modulating network state

Neuron

Volumn 79, Issue 3, 2013, Pages 567-578

  Zagha, Edward ^a   Casale, Amanda E ^a   Sachdev, Robert N S ^a   McGinley, Matthew J ^a   McCormick, David A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; EVOKED SOMATOSENSORY RESPONSE; EXCITATION; FEEDBACK SYSTEM; MOUSE; NETWORK STATE; NEUROMODULATION; NONHUMAN; OPTOGENETICS; PRIMARY MOTOR CORTEX; PRIMARY SOMATOSENSORY CORTEX; PRIORITY JOURNAL; SENSORY PROCESSING; THALAMUS; VIBRISSA;

ACTION POTENTIALS; ANESTHESIA; ANIMALS; BRAIN MAPPING; ELECTROMYOGRAPHY; FEEDBACK, PHYSIOLOGICAL; HOMEODOMAIN PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR CORTEX; NERVE NET; NONLINEAR DYNAMICS; OPTOGENETICS; RHODOPSIN; SENSATION; SOMATOSENSORY CORTEX; TRANSCRIPTION FACTORS; VIBRISSAE;

EID: 84881496012     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.06.008     Document Type: Article

References (64)

1. Arieli A., Sterkin A., Grinvald A., Aertsen A. Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 1996, 273:1868-1871.
2. Berger H. Über das Elektroenkephalogramm des Menschen. Arch. Psychiatr. Nervenkr. 1929, 87:527-570.
3. Borisovska M., McGinley M.J., Bensen A., Westbrook G.L. Loss of olfactory cell adhesion molecule reduces the synchrony of mitral cell activity in olfactory glomeruli. J.Physiol. 2011, 589:1927-1941.
4. Brecht M. Movement, confusion, and orienting in frontal cortices. Neuron 2011, 72:193-196.
5. Buzsaki G. Rhythms of the Brain 2006, Oxford University Press, New York.
6. Buzsaki G., Bickford R.G., Ponomareff G., Thal L.J., Mandel R., Gage F.H. Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J.Neurosci. 1988, 8:4007-4026.
7. Carvell G.E., Miller S.A., Simons D.J. The relationship of vibrissal motor cortex unit activity to whisking in the awake rat. Somatosens. Mot. Res. 1996, 13:115-127.
8. Cauller L. Layer I of primary sensory neocortex: where top-down converges upon bottom-up. Behav. Brain Res. 1995, 71:163-170.
9. Cauller L.J., Kulics A.T. The neural basis of the behaviorally relevant N1 component of the somatosensory-evoked potential in SI cortex of awake monkeys: evidence that backward cortical projections signal conscious touch sensation. Exp. Brain Res. 1991, 84:607-619.
10. Churchland M.M., Cunningham J.P., Kaufman M.T., Ryu S.I., Shenoy K.V. Cortical preparatory activity: representation of movement or first cog in a dynamical machine?. Neuron 2010, 68:387-400.
11. Constantinople C.M., Bruno R.M. Effects and mechanisms of wakefulness on local cortical networks. Neuron 2011, 69:1061-1068.
12. Crochet S., Petersen C.C. Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nat. Neurosci. 2006, 9:608-610.
13. Di S., Baumgartner C., Barth D.S. Laminar analysis of extracellular field potentials in rat vibrissa/barrel cortex. J.Neurophysiol. 1990, 63:832-840.
14. Dringenberg H.C., Vanderwolf C.H. Neocortical activation: modulation by multiple pathways acting on central cholinergic and serotonergic systems. Exp. Brain Res. 1997, 116:160-174.
15. Engel A.K., Fries P., Singer W. Dynamic predictions: oscillations and synchrony in top-down processing. Nat. Rev. Neurosci. 2001, 2:704-716.
16. Erlich J.C., Bialek M., Brody C.D. A cortical substrate for memory-guided orienting in the rat. Neuron 2011, 72:330-343.
17. Fanselow E.E., Nicolelis M.A. Behavioral modulation of tactile responses in the rat somatosensory system. J.Neurosci. 1999, 19:7603-7616.
18. Felleman D.J., Van Essen D.C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1991, 1:1-47.
19. Ferezou I., Haiss F., Gentet L.J., Aronoff R., Weber B., Petersen C.C. Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice. Neuron 2007, 56:907-923.
20. Friedman W.A., Zeigler H.P., Keller A. Vibrissae motor cortex unit activity during whisking. J.Neurophysiol. 2012, 107:551-563.
21. Fries P., Reynolds J.H., Rorie A.E., Desimone R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 2001, 291:1560-1563.
22. Gazzaley A., Nobre A.C. Top-down modulation: bridging selective attention and working memory. Trends Cogn. Sci. 2012, 16:129-135.
23. Goard M., Dan Y. Basal forebrain activation enhances cortical coding of natural scenes. Nat. Neurosci. 2009, 12:1444-1449.
24. Haider B., McCormick D.A. Rapid neocortical dynamics: cellular and network mechanisms. Neuron 2009, 62:171-189.
25. Haider B., Duque A., Hasenstaub A.R., Yu Y., McCormick D.A. Enhancement of visual responsiveness by spontaneous local network activity invivo. J.Neurophysiol. 2007, 97:4186-4202.
26. Harris K.D., Thiele A. Cortical state and attention. Nat. Rev. Neurosci. 2011, 12:509-523.
27. Hasenstaub A., Sachdev R.N., McCormick D.A. State changes rapidly modulate cortical neuronal responsiveness. J.Neurosci. 2007, 27:9607-9622.
28. Hentschke H., Haiss F., Schwarz C. Central signals rapidly switch tactile processing in rat barrel cortex during whisker movements. Cereb. Cortex 2006, 16:1142-1156.
29. Hill D.N., Curtis J.C., Moore J.D., Kleinfeld D. Primary motor cortex reports efferent control of vibrissa motion on multiple timescales. Neuron 2011, 72:344-356.
30. Huber D., Gutnisky D.A., Peron S., O'Connor D.H., Wiegert J.S., Tian L., Oertner T.G., Looger L.L., Svoboda K. Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 2012, 484:473-478.
31. Jones B.E. Arousal systems. Front. Biosci. 2003, 8:s438-s451.
32. Kleinfeld D., Berg R.W., O'Connor S.M. Anatomical loops and their electrical dynamics in relation to whisking by rat. Somatosens. Mot. Res. 1999, 16:69-88.
33. Kleinfeld D., Ahissar E., Diamond M.E. Active sensation: insights from the rodent vibrissa sensorimotor system. Curr. Opin. Neurobiol. 2006, 16:435-444.
34. Krupa D.J., Wiest M.C., Shuler M.G., Laubach M., Nicolelis M.A. Layer-specific somatosensory cortical activation during active tactile discrimination. Science 2004, 304:1989-1992.
35. Lamme V.A., Roelfsema P.R. The distinct modes of vision offered by feedforward and recurrent processing. Trends Neurosci. 2000, 23:571-579.
36. Larkum M.E., Zhu J.J. Signaling of layer 1 and whisker-evoked Ca2+ and Na+ action potentials in distal and terminal dendrites of rat neocortical pyramidal neurons invitro and invivo. J.Neurosci. 2002, 22:6991-7005.
37. Lee S.H., Dan Y. Neuromodulation of brain states. Neuron 2012, 76:209-222.
38. Lee S., Carvell G.E., Simons D.J. Motor modulation of afferent somatosensory circuits. Nat. Neurosci. 2008, 11:1430-1438.
39. Margrie T.W., Brecht M., Sakmann B. Invivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain. Pflugers Arch. 2002, 444:491-498.
40. Marguet S.L., Harris K.D. State-dependent representation of amplitude-modulated noise stimuli in rat auditory cortex. J.Neurosci. 2011, 31:6414-6420.
41. McCormick D.A., von Krosigk M. Corticothalamic activation modulates thalamic firing through glutamate "metabotropic" receptors. Proc. Natl. Acad. Sci. USA 1992, 89:2774-2778.
42. McCormick D.A., Wang Z., Huguenard J. Neurotransmitter control of neocortical neuronal activity and excitability. Cereb. Cortex 1993, 3:387-398.
43. Metherate R., Cox C.L., Ashe J.H. Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J.Neurosci. 1992, 12:4701-4711.
44. Miyashita E., Keller A., Asanuma H. Input-output organization of the rat vibrissal motor cortex. Exp. Brain Res. 1994, 99:223-232.
45. Moran J., Desimone R. Selective attention gates visual processing in the extrastriate cortex. Science 1985, 229:782-784.
46. Moruzzi G., Magoun H.W. Brain stem reticular formation and activation of the EEG. Electroencephalogr. Clin. Neurophysiol. 1949, 1:455-473.
47. Nicolelis M.A., Fanselow E.E. Thalamocortical [correction of Thalamcortical] optimization of tactile processing according to behavioral state. Nat. Neurosci. 2002, 5:517-523.
48. Niell C.M., Stryker M.P. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 2010, 65:472-479.
49. Petersen C.C., Hahn T.T., Mehta M., Grinvald A., Sakmann B. Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc. Natl. Acad. Sci. USA 2003, 100:13638-13643.
50. Petreanu L., Mao T., Sternson S.M., Svoboda K. The subcellular organization of neocortical excitatory connections. Nature 2009, 457:1142-1145.
51. Petreanu L., Gutnisky D.A., Huber D., Xu N.L., O'Connor D.H., Tian L., Looger L., Svoboda K. Activity in motor-sensory projections reveals distributed coding in somatosensation. Nature 2012, 489:299-303.
52. Porter L.L., White E.L. Afferent and efferent pathways of the vibrissal region of primary motor cortex in the mouse. J.Comp. Neurol. 1983, 214:279-289.
53. Poulet J.F., Petersen C.C. Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 2008, 454:881-885.
54. Poulet J.F., Fernandez L.M., Crochet S., Petersen C.C. Thalamic control of cortical states. Nat. Neurosci. 2012, 15:370-372.
55. Reynolds J.H., Chelazzi L. Attentional modulation of visual processing. Annu. Rev. Neurosci. 2004, 27:611-647.
56. Rocco M.M., Brumberg J.C. The sensorimotor slice. J.Neurosci. Methods 2007, 162:139-147.
57. Sachdev R.N., Ebner F.F., Wilson C.J. Effect of subthreshold up and down states on the whisker-evoked response in somatosensory cortex. J.Neurophysiol. 2004, 92:3511-3521.
58. Sharp F.R., Evans K. Regional (14C) 2-deoxyglucose uptake during vibrissae movements evoked by rat motor cortex stimulation. J.Comp. Neurol. 1982, 208:255-287.
59. Steriade M., Amzica F., Nuñez A. Cholinergic and noradrenergic modulation of the slow (approximately 0.3Hz) oscillation in neocortical cells. J.Neurophysiol. 1993, 70:1385-1400.
60. Steriade M., McCormick D.A., Sejnowski T.J. Thalamocortical oscillations in the sleeping and aroused brain. Science 1993, 262:679-685.
61. Steriade M., Nuñez A., Amzica F. A novel slow (< 1Hz) oscillation of neocortical neurons invivo: depolarizing and hyperpolarizing components. J.Neurosci. 1993, 13:3252-3265.
62. Tanji J., Evarts E.V. Anticipatory activity of motor cortex neurons in relation to direction of an intended movement. J.Neurophysiol. 1976, 39:1062-1068.
63. Veinante P., Deschênes M. Single-cell study of motor cortex projections to the barrel field in rats. J.Comp. Neurol. 2003, 464:98-103.
64. Wolfart J., Debay D., Le Masson G., Destexhe A., Bal T. Synaptic background activity controls spike transfer from thalamus to cortex. Nat. Neurosci. 2005, 8:1760-1767.