A Corticothalamic Switch: Controlling the Thalamus with Dynamic Synapses

Neuron

Volumn 86, Issue 3, 2015, Pages 768-782

  Crandall, Shane R ^a   Cruikshank, Scott J ^a   Connors, Barry W ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; CONTROLLED STUDY; CORTICOTHALAMIC NEURON; FEMALE; FREQUENCY MODULATION; GAMMA RHYTHM; MALE; MOUSE; NERVE CELL; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NEUROANATOMY; NEUROPSYCHOLOGY; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; REGULATORY MECHANISM; SENSORY NERVE; THALAMUS; ANALOGS AND DERIVATIVES; ANIMAL; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; IN VITRO STUDY; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; NERVE TRACT; OPTOGENETICS; PHYSIOLOGY; SOMATOSENSORY CORTEX; SYNAPSE; TRANSGENIC MOUSE;

2-AMINO-5-PHOSPHOPENTANOIC ACID; 4 AMINOBUTYRIC ACID; AMINO ACID RECEPTOR BLOCKING AGENT; BACTERIAL PROTEIN; CENTRAL STIMULANT AGENT; CHANNELRHODOPSIN 2, MOUSE; N METHYLASPARTIC ACID; NEUROTENSIN RECEPTOR; NEUROTENSIN TYPE 1 RECEPTOR; PHOTOPROTEIN; PICROTOXIN; RHODOPSIN; VALINE; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ANIMALS; BACTERIAL PROTEINS; CENTRAL NERVOUS SYSTEM STIMULANTS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GAMMA-AMINOBUTYRIC ACID; IN VITRO TECHNIQUES; LUMINESCENT PROTEINS; MICE; MICE, INBRED ICR; MICE, TRANSGENIC; N-METHYLASPARTATE; NEURAL PATHWAYS; OPTOGENETICS; PICROTOXIN; RECEPTORS, NEUROTENSIN; RHODOPSIN; SOMATOSENSORY CORTEX; SYNAPSES; THALAMUS; VALINE;

EID: 84928980797     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.03.040     Document Type: Article

References (88)

1. Adesnik H., Scanziani M. Lateral competition for cortical space by layer-specific horizontal circuits. Nature 2010, 464:1155-1160.
2. Agmon A., Connors B.W. Thalamocortical responses of mouse somatosensory (barrel) cortex invitro. Neuroscience 1991, 41:365-379.
3. Alonso J.M., Usrey W.M., Reid R.C. Precisely correlated firing in cells of the lateral geniculate nucleus. Nature 1996, 383:815-819.
4. Arcelli P., Frassoni C., Regondi M.C., De Biasi S., Spreafico R. GABAergic neurons in mammalian thalamus: a marker of thalamic complexity?. Brain Res. Bull. 1997, 42:27-37.
5. Augustinaite S., Kuhn B., Helm P.J., Heggelund P. NMDA spike/plateau potentials in dendrites of thalamocortical neurons. J.Neurosci. 2014, 34:10892-10905.
6. Bastos A.M., Briggs F., Alitto H.J., Mangun G.R., Usrey W.M. Simultaneous recordings from the primary visual cortex and lateral geniculate nucleus reveal rhythmic interactions and a cortical source for γ-band oscillations. J.Neurosci. 2014, 34:7639-7644.
7. Beierlein M., Connors B.W. Short-term dynamics of thalamocortical and intracortical synapses onto layer 6 neurons in neocortex. J.Neurophysiol. 2002, 88:1924-1932.
8. 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.
9. Bourassa J., Pinault D., Deschênes M. Corticothalamic projections from the cortical barrel field to the somatosensory thalamus in rats: a single-fibre study using biocytin as an anterograde tracer. Eur. J. Neurosci. 1995, 7:19-30.
10. Briggs F., Usrey W.M. Emerging views of corticothalamic function. Curr. Opin. Neurobiol. 2008, 18:403-407.
11. Briggs F., Usrey W.M. Modulation of gamma-band activity across local cortical circuits. Front. Integr. Neurosci. 2009, 3:15.
12. Briggs F., Usrey W.M. Parallel processing in the corticogeniculate pathway of the macaque monkey. Neuron 2009, 62:135-146.
13. Bruno R.M., Sakmann B. Cortex is driven by weak but synchronously active thalamocortical synapses. Science 2006, 312:1622-1627.
14. Cardin J.A., Carlén M., Meletis K., Knoblich U., Zhang F., Deisseroth K., Tsai L.H., Moore C.I. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 2009, 459:663-667.
15. Castro-Alamancos M.A. Properties of primary sensory (lemniscal) synapses in the ventrobasal thalamus and the relay of high-frequency sensory inputs. J.Neurophysiol. 2002, 87:946-953.
16. Cox C.L. Complex regulation of dendritic transmitter release from thalamic interneurons. Curr. Opin. Neurobiol. 2014, 29:126-132.
17. Cox C.L., Huguenard J.R., Prince D.A. Nucleus reticularis neurons mediate diverse inhibitory effects in thalamus. Proc. Natl. Acad. Sci. USA 1997, 94:8854-8859.
18. Crandall S.R., Govindaiah G., Cox C.L. Low-threshold Ca2+ current amplifies distal dendritic signaling in thalamic reticular neurons. J.Neurosci. 2010, 30:15419-15429.
19. Cruikshank S.J., Lewis T.J., Connors B.W. Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nat. Neurosci. 2007, 10:462-468.
20. Cruikshank S.J., Urabe H., Nurmikko A.V., Connors B.W. Pathway-specific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons. Neuron 2010, 65:230-245.
21. Crunelli V., Lightowler S., Pollard C.E. A T-type Ca2+ current underlies low-threshold Ca2+ potentials in cells of the cat and rat lateral geniculate nucleus. J.Physiol. 1989, 413:543-561.
22. Cudeiro J., Sillito A.M. Looking back: corticothalamic feedback and early visual processing. Trends Neurosci. 2006, 29:298-306.
23. Deschênes M., Hu B. Electrophysiology and pharmacology of the corticothalamic input to lateral thalamic nuclei: an intracellular study in the cat. Eur. J. Neurosci. 1990, 2:140-152.
24. Deschênes M., Veinante P., Zhang Z.W. The organization of corticothalamic projections: reciprocity versus parity. Brain Res. Brain Res. Rev. 1998, 28:286-308.
25. Diamond M.E., Armstrong-James M., Budway M.J., Ebner F.F. Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus: dependence on the barrel field cortex. J.Comp. Neurol. 1992, 319:66-84.
26. Diamond M.E., von Heimendahl M., Knutsen P.M., Kleinfeld D., Ahissar E. 'Where' and 'what' in the whisker sensorimotor system. Nat. Rev. Neurosci. 2008, 9:601-612.
27. Erişir A., Van Horn S.C., Sherman S.M. Relative numbers of cortical and brainstem inputs to the lateral geniculate nucleus. Proc. Natl. Acad. Sci. USA 1997, 94:1517-1520.
28. Ferster D., Lindström S. Augmenting responses evoked in area 17of the cat by intracortical axon collaterals of cortico-geniculate cells. J.Physiol. 1985, 367:217-232.
29. Fries P. Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu. Rev. Neurosci. 2009, 32:209-224.
30. Ghosh S., Murray G.M., Turman A.B., Rowe M.J. Corticothalamic influences on transmission of tactile information in the ventroposterolateral thalamus of the cat: effect of reversible inactivation of somatosensory cortical areas I and II. Exp. Brain Res. 1994, 100:276-286.
31. Golshani P., Liu X.B., Jones E.G. Differences in quantal amplitude reflect GluR4- subunit number at corticothalamic synapses on two populations of thalamic neurons. Proc. Natl. Acad. Sci. USA 2001, 98:4172-4177.
32. 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.
33. Guido W., Weyand T. Burst responses in thalamic relay cells of the awake behaving cat. J.Neurophysiol. 1995, 74:1782-1786.
34. Guillery R.W., Harting J.K. Structure and connections of the thalamic reticular nucleus: advancing views over half a century. J.Comp. Neurol. 2003, 463:360-371.
35. Hirsch J.C., Fourment A., Marc M.E. Sleep-related variations of membrane potential in the lateral geniculate body relay neurons of the cat. Brain Res. 1983, 259:308-312.
36. Huguenard J.R., Prince D.A. A novel T-type current underlies prolonged Ca(2+)-dependent burst firing in GABAergic neurons of rat thalamic reticular nucleus. J.Neurosci. 1992, 12:3804-3817.
37. Huguenard J.R., McCormick D.A. Thalamic synchrony and dynamic regulation of global forebrain oscillations. Trends Neurosci. 2007, 30:350-356.
38. Huntsman M.M., Porcello D.M., Homanics G.E., DeLorey T.M., Huguenard J.R. Reciprocal inhibitory connections and network synchrony in the mammalian thalamus. Science 1999, 283:541-543.
39. Jahnsen H., Llinás R. Electrophysiological properties of guinea-pig thalamic neurones: an invitro study. J.Physiol. 1984, 349:205-226.
40. Jurgens C.W., Bell K.A., McQuiston A.R., Guido W. Optogenetic stimulation of the corticothalamic pathway affects relay cells and GABAergic neurons differently in the mouse visual thalamus. PLoS ONE 2012, 7:e45717.
41. Kao C.Q., Coulter D.A. Physiology and pharmacology of corticothalamic stimulation-evoked responses in rat somatosensory thalamic neurons invitro. J.Neurophysiol. 1997, 77:2661-2676.
42. Kim U., Sanchez-Vives M.V., McCormick D.A. Functional dynamics of GABAergic inhibition in the thalamus. Science 1997, 278:130-134.
43. 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.
44. Kwegyir-Afful E.E., Simons D.J. Subthreshold receptive field properties distinguish different classes of corticothalamic neurons in the somatosensory system. J.Neurosci. 2009, 29:964-972.
45. Lam Y.W., Sherman S.M. Functional organization of the somatosensory cortical layer 6 feedback to the thalamus. Cereb. Cortex 2010, 20:13-24.
46. Landisman C.E., Connors B.W. VPM and PoM nuclei of the rat somatosensory thalamus: intrinsic neuronal properties and corticothalamic feedback. Cereb. Cortex 2007, 17:2853-2865.
47. Landisman C.E., Long M.A., Beierlein M., Deans M.R., Paul D.L., Connors B.W. Electrical synapses in the thalamic reticular nucleus. J.Neurosci. 2002, 22:1002-1009.
48. Landry P., Dykes R.W. Identification of two populations of corticothalamic neurons in cat primary somatosensory cortex. Exp. Brain Res. 1985, 60:289-298.
49. Lee S., Carvell G.E., Simons D.J. Motor modulation of afferent somatosensory circuits. Nat. Neurosci. 2008, 11:1430-1438.
50. Leresche N., Lambert R.C., Errington A.C., Crunelli V. From sleep spindles of natural sleep to spike and wave discharges of typical absence seizures: is the hypothesis still valid?. Pflugers Arch. 2012, 463:201-212.
51. Li L., Ebner F.F. Cortical modulation of spatial and angular tuning maps in the rat thalamus. J.Neurosci. 2007, 27:167-179.
52. Liu X.B., Honda C.N., Jones E.G. Distribution of four types of synapse on physiologically identified relay neurons in the ventral posterior thalamic nucleus of the cat. J.Comp. Neurol. 1995, 352:69-91.
53. Llinás R., Ribary U., Contreras D., Pedroarena C. The neuronal basis for consciousness. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1998, 353:1841-1849.
54. MacDermott A.B., Dale N. Receptors, ion channels and synaptic potentials underlying the integrative actions of excitatory amino acids. Trends Neurosci. 1987, 10:280-284.
55. Mayer M.L., Westbrook G.L., Guthrie P.B. Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones. Nature 1984, 309:261-263.
56. McAlonan K., Cavanaugh J., Wurtz R.H. Guarding the gateway to cortex with attention in visual thalamus. Nature 2008, 456:391-394.
57. McCormick D.A., Feeser H.R. Functional implications of burstfiring and single spike activity in lateral geniculate relay neurons. Neuroscience 1990, 39:103-113.
58. Mease R.A., Krieger P., Groh A. Cortical control of adaptation and sensory relay mode in the thalamus. Proc. Natl. Acad. Sci. USA 2014, 111:6798-6803.
59. Miyata M. Distinct properties of corticothalamic and primary sensory synapses to thalamic neurons. Neurosci. Res. 2007, 59:377-382.
60. Normand E.A., Crandall S.R., Thorn C.A., Murphy E.M., Voelcker B., Browning C., Machan J.T., Moore C.I., Connors B.W., Zervas M. Temporal and mosaic Tsc1 deletion in the developing thalamus disrupts thalamocortical circuitry, neural function, and behavior. Neuron 2013, 78:895-909.
61. Nowak L., Bregestovski P., Ascher P., Herbet A., Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 1984, 307:462-465.
62. O'Connor D.H., Fukui M.M., Pinsk M.A., Kastner S. Attention modulates responses in the human lateral geniculate nucleus. Nat. Neurosci. 2002, 5:1203-1209.
63. O'Connor D.H., Peron S.P., Huber D., Svoboda K. Neural activity in barrel cortex underlying vibrissa-based object localization in mice. Neuron 2010, 67:1048-1061.
64. 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.
65. Paz J.T., Bryant A.S., Peng K., Fenno L., Yizhar O., Frankel W.N., Deisseroth K., Huguenard J.R. A new mode of corticothalamic transmission revealed in the Gria4(-/-) model of absence epilepsy. Nat. Neurosci. 2011, 14:1167-1173.
66. Pedroarena C.M., Llinás R. Interactions of synaptic and intrinsic electroresponsiveness determine corticothalamic activation dynamics. Thalamus Relat. Syst. 2001, 1:3-14.
67. Prinz A.A., Abbott L.F., Marder E. The dynamic clamp comes of age. Trends Neurosci. 2004, 27:218-224.
68. Scharfman H.E., Lu S.M., Guido W., Adams P.R., Sherman S.M. N-methyl-D-aspartate receptors contribute to excitatory postsynaptic potentials of cat lateral geniculate neurons recorded in thalamic slices. Proc. Natl. Acad. Sci. USA 1990, 87:4548-4552.
69. Sherman S.M., Koch C. The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus. Exp. Brain Res. 1986, 63:1-20.
70. Siegle J.H., Pritchett D.L., Moore C.I. Gamma-range synchronization of fast-spiking interneurons can enhance detection of tactile stimuli. Nat. Neurosci. 2014, 17:1371-1379.
71. Sillito A.M., Jones H.E., Gerstein G.L., West D.C. Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex. Nature 1994, 369:479-482.
72. Singer W. Synchronization of cortical activity and its putative role in information processing and learning. Annu. Rev. Physiol. 1993, 55:349-374.
73. Steriade M., McCormick D.A., Sejnowski T.J. Thalamocortical oscillations in the sleeping and aroused brain. Science 1993, 262:679-685.
74. Steriade M., Contreras D., Amzica F., Timofeev I. Synchronization of fast (30-40Hz) spontaneous oscillations in intrathalamic and thalamocortical networks. J.Neurosci. 1996, 16:2788-2808.
75. Sun Y.G., Beierlein M. Receptor saturation controls short-term synaptic plasticity at corticothalamic synapses. J.Neurophysiol. 2011, 105:2319-2329.
76. Swadlow H.A. Efferent neurons and suspected interneurons in S-1 vibrissa cortex of the awake rabbit: receptive fields and axonal properties. J.Neurophysiol. 1989, 62:288-308.
77. Swadlow H.A., Weyand T.G. Corticogeniculate neurons, corticotectal neurons, and suspected interneurons in visual cortex of awake rabbits: receptive-field properties, axonal properties, and effects of EEG arousal. J.Neurophysiol. 1987, 57:977-1001.
78. Swadlow H.A., Gusev A.G. The impact of 'bursting' thalamic impulses at a neocortical synapse. Nat. Neurosci. 2001, 4:402-408.
79. Temereanca S., Simons D.J. Functional topography of corticothalamic feedback enhances thalamic spatial response tuning in the somatosensory whisker/barrel system. Neuron 2004, 41:639-651.
80. Turner J.P., Salt T.E. Characterization of sensory and corticothalamic excitatory inputs to rat thalamocortical neurones invitro. J.Physiol. 1998, 510:829-843.
81. Usrey W.M., Alonso J.M., Reid R.C. Synaptic interactions between thalamic inputs to simple cells in cat visual cortex. J.Neurosci. 2000, 20:5461-5467.
82. Van Horn S.C., Erişir A., Sherman S.M. Relative distribution ofsynapses in the A-laminae of the lateral geniculate nucleus of the cat. J.Comp. Neurol. 2000, 416:509-520.
83. von Krosigk M., Monckton J.E., Reiner P.B., McCormick D.A. Dynamic properties of corticothalamic excitatory postsynaptic potentials and thalamic reticular inhibitory postsynaptic potentials in thalamocortical neurons of the guinea-pig dorsal lateral geniculate nucleus. Neuroscience 1999, 91:7-20.
84. Wang X., Sommer F.T., Hirsch J.A. Inhibitory circuits for visual processing in thalamus. Curr. Opin. Neurobiol. 2011, 21:726-733.
85. Yang Q., Chen C.C., Ramos R.L., Katz E., Keller A., Brumberg J.C. Intrinsic properties of and thalamocortical inputs onto identified corticothalamic-VPM neurons. Somatosens. Mot. Res. 2014, 31:78-93.
86. Yuan B., Morrow T.J., Casey K.L. Corticofugal influences of S1 cortex on ventrobasal thalamic neurons in the awake rat. J.Neurosci. 1986, 6:3611-3617.
87. Zhou Y., Liu B.H., Wu G.K., Kim Y.J., Xiao Z., Tao H.W., Zhang L.I. Preceding inhibition silences layer 6 neurons in auditory cortex. Neuron 2010, 65:706-717.
88. Zucker R.S., Regehr W.G. Short-term synaptic plasticity. Annu. Rev. Physiol. 2002, 64:355-405.