Thalamocortical up states: Differential effects of intrinsic and extrinsic cortical inputs on persistent activity

Journal of Neuroscience

Volumn 27, Issue 16, 2007, Pages 4261-4272

  Rigas, Pavlos ^a   Castro Alamancos, Manuel A ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Arousal; Cortex; Down state; Slow oscillation; Thalamocortical slice; Thalamus

Indexed keywords

ANIMAL TISSUE; AROUSAL; ARTICLE; BRAIN CORTEX; BRAIN DEPTH STIMULATION; BRAIN SLICE; CONTROLLED STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; THALAMOCORTICAL TRACT; THALAMUS;

ACTION POTENTIALS; AFFECT; ANIMALS; AROUSAL; CEREBRAL CORTEX; MEMBRANE POTENTIALS; MICE; MICE, INBRED BALB C; NERVE NET; PATCH-CLAMP TECHNIQUES; THALAMUS;

EID: 34247360027     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0003-07.2007     Document Type: Article

References (65)

1. Agmon A, Connors BW (1991) Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41:365-379.
2. Alonso JM, Usrey WM, Reid RC (1996) Precisely correlated firing in cells of the lateral geniculate nucleus. Nature 383:815-819.
3. Anderson J, Lampl I, Reichova I, Carandini M, Ferster D (2000) Stimulus dependence of two-state fluctuations of membrane potential in cat visual cortex. Nat Neurosci 3:617-621.
4. Benshalom G, White EL (1986) Quantification of thalamocortical synapses with spiny stellate neurons in layer IV of mouse somatosensory cortex. J Comp Neurol 253:303-314.
5. Bezdudnaya T, Cano M, Bereshpolova Y, Stoelzel CR, Alonso JM, Swadlow HA (2006) Thalamic burst mode and inattention in the awake LGNd. Neuron 49:421-432.
6. Boudreau CE, Ferster D (2005) Short-term depression in thalamocortical synapses of cat primary visual cortex. J Neurosci 25:7179-7190.
7. Brecht M, Sakmann B (2002) Dynamic representation of whisker deflection by synaptic potentials in spiny stellate and pyramidal cells in the barrels and septa of layer 4 rat somatosensory cortex. J Physiol (Lond) 543:49-70.
8. Bruno RM, Sakmann B (2006) Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312:1622-1627.
9. Bruno RM, Simons DJ (2002) Feedforward mechanisms of excitatory and inhibitory cortical receptive fields. J Neurosci 22:10966-10975.
10. Castro-Alamancos MA (2002a) Different temporal processing of sensory inputs in the rat thalamus during quiescent and information processing states in vivo. J Physiol (Lond) 539:567-578.
11. Castro-Alamancos MA (2002b) Role of thalamocortical sensory suppression during arousal: focusing sensory inputs in neocortex. J Neurosci 22:9651-9655.
12. Castro-Alamancos MA (2004a) Absence of rapid sensory adaptation in neocortex during information processing states. Neuron 41:455-464.
13. Castro-Alamancos MA (2004b) Dynamics of sensory thalamocortical synaptic networks during information processing states. Prog Neurobiol 74:213-247.
14. Castro-Alamancos MA, Calcagnotto ME (1999) Presynaptic long-term potentiation in corticothalamic synapses. J Neurosci 19:9090-9097.
15. Castro-Alamancos MA, Calcagnotto ME (2001) High-pass filtering of corticothalamic activity by neuromodulators released in the thalamus during arousal: in vitro and in vivo. J Neurophysiol 85:1489-1497.
16. Castro-Alamancos MA, Connors BW (1996a) Short-term plasticity of a thalamocortical pathway dynamically modulated by behavioral state. Science 272:274-277.
17. Castro-Alamancos MA, Connors BW (1996b) Cellular mechanisms of the augmenting response: short-term plasticity in a thalamocortical pathway. J Neurosci 16:7742-7756.
18. Castro-Alamancos MA, Connors BW (1997) Thalamocortical synapses. Prog Neurobiol 51:581-606.
19. Castro-Alamancos MA, Oldford E (2002) Cortical sensory suppression during arousal is due to the activity-dependent depression of thalamocortical synapses. J Physiol (Lond) 541:319-331.
20. Castro-Alamancos MA, Rigas P (2002) Synchronized oscillations caused by disinhibition in rodent neocortex are generated by recurrent synaptic activity mediated by AMPA receptors. J Physiol (Lond) 542:567-581.
21. Castro-Alamancos MA, Rigas P, Tawara-Hirata Y (2006) Resonance (̃10 Hz) of excitatory networks in motor cortex: effects of voltage-dependent ion channel blockers. J Physiol (Lond) 578:173-191.
22. Chung S, Li X, Nelson SB (2002) Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo. Neuron 34:437-446.
23. Contreras D, Steriade M (1995) Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J Neurosci 15:604-622.
24. Cowan RL, Wilson CJ (1994) Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. J Neurophysiol 71:17-32.
25. Cunningham MO, Pervouchine DD, Racca C, Kopell NJ, Davies CH, Jones RS, Traub RD, Whittington MA (2006) Neuronal metabolism governs cortical network response state. Proc Natl Acad Sci USA 103:5597-5601.
26. Destexhe A, Rudolph M, Pare D (2003) The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci 4:739-751.
27. Douglas RJ, Koch C, Mahowald M, Martin KA, Suarez HH (1995) Recurrent excitation in neocortical circuits. Science 269:981-985.
28. Fanselow EE, Nicolelis MA (1999) Behavioral modulation of tactile responses in the rat somatosensory system. J Neurosci 19:7603-7616.
29. Ferster D, Lindstrom S (1985) Synaptic excitation of neurones in area 17 of the cat by intracortical axon collaterals of cortico-geniculate cells. J Physiol (Lond) 367:233-252.
30. Gabernet L, Jadhav SP, Feldman DE, Carandini M, Scanziani M (2005) Somatosensory integration controlled by dynamic thalamocortical feedforward inhibition. Neuron 48:315-327.
31. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75-79.
32. Gil Z, Connors BW, Amitai Y (1997) Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19:679-686.
33. Grenier F, Timofeev I, Steriade M (1998) Leading role of thalamic over cortical neurons during postinhibitory rebound excitation. Proc Natl Acad Sci USA 95:13929-13934.
34. Guillery RW (1971) Patterns of synaptic interconnections in the dorsal lateral geniculate nucleus of cat and monkey: a brief review. Vision Res [Suppl] 3:211-227.
35. Hasenstaub A, Shu Y, Haider B, Kraushaar U, Duque A, McCormick DA (2005) Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 47:423-435.
36. Hirata A, Castro-Alamancos MA (2006) Relief of synaptic depression produces long-term enhancement in thalamocortical networks. J Neurophysiol 95:2479-2491.
37. Hirata A, Aguilar J, Castro-Alamancos MA (2006) Noradrenergic activation amplifies bottom-up and top-down signal-to-noise ratios in sensory thalamus. J Neurosci 26:4426-4436.
38. Hughes SW, Cope DW, Blethyn KL, Crunelli V (2002) Cellular mechanisms of the slow (<1 Hz) oscillation in thalamocortical neurons in vitro. Neuron 33:947-958.
39. Kao CQ, Coulter DA (1997) Physiology and pharmacology of corticothalamic stimulation-evoked responses in rat somatosensory thalamic neurons in vitro. J Neurophysiol 77:2661-2676.
40. MacLean JN, Watson BO, Aaron GB, Yuste R (2005) Internal dynamics determine the cortical response to thalamic stimulation. Neuron 48:811-823.
41. Mao BQ, Hamzei-Sichani F, Aronov D, Froemke RC, Yuste R (2001) Dynamics of spontaneous activity in neocortical slices. Neuron 32:883-898.
42. McCormick DA, Shu Y, Hasenstaub A, Sanchez-Vives M, Badoual M, Bal T (2003) Persistent cortical activity: mechanisms of generation and effects on neuronal excitability. Cereb Cortex 13:1219-1231.
43. Metherate R, Ashe JH (1993) Ionic flux contributions to neocortical slow waves and nucleus basalis-mediated activation: whole-cell recordings in vivo. J Neurosci 13:5312-5323.
44. Moore CI, Nelson SB, Sur M (1999) Dynamics of neuronal processing in rat somatosensory cortex. Trends Neurosci 22:513-520.
45. Moruzzi G, Magoun HW (1949) Brain stem reticular formation and activation of the EEG. Electroencephalogr Clin Neurophysiol 1:455-473.
46. Oldford E, Castro-Alamancos MA (2003) Input-specific effects of acetylcholine on sensory and intracortical evoked responses in the "barrel cortex" in vivo. Neuroscience 117:769-778.
47. Petersen CC, Hahn TT, Mehta M, Grinvald A, Sakmann B (2003) Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci USA 100:13638-13643.
48. Pinto DJ, Hartings JA, Brumberg JC, Simons DJ (2003) Cortical damping: analysis of thalamocortical response transformations in rodent barrel cortex. Cereb Cortex 13:33-44.
49. Rudolph M, Pelletier JG, Pare D, Destexhe A (2005) Characterization of synaptic conductances and integrative properties during electrically induced EEG-activated states in neocortical neurons in vivo. J Neurophysiol 94:2805-2821.
50. Sanchez-Vives MV, McCormick DA (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3:1027-1034.
51. Sherman SM (2001) A wake-up call from the thalamus. Nat Neurosci 4:344-346.
52. Sherman SM, Guillery RW (1996) Functional organization of thalamocortical relays. J Neurophysiol 76:1367-1395.
53. Shu Y, Hasenstaub A, McCormick DA (2003) Turning on and off recurrent balanced cortical activity. Nature 423:288-293.
54. Steriade M, Oakson G, Kitsikis A (1978) Firing rates and patterns of output and nonoutput cells in cortical areas 5 and 7 of cat during the sleepwaking cycle. Exp Neurol 60:443-468.
55. Steriade M, Nunez A, Amzica F (1993a) A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci 13:3252-3265.
56. Steriade M, Nunez A, Amzica F (1993b) Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci 13:3266-3283.
57. Steriade M, Contreras D, Curro DR, Nunez A (1993c) The slow (<1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks. J Neurosci 13:3284-3299.
58. Steriade M, McCormick DA, Sejnowski TJ (1993d) Thalamocortical oscillations in the sleeping and aroused brain. Science 262:679-685.
59. Steriade M, Jones EG, McCormick DA (1997) Thalamus. New York: Elsevier.
60. Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85:1969-1985.
61. Sun QQ, Huguenard JR, Prince DA (2006) Barrel cortex microcircuits: thalamocortical feedforward inhibition in spiny stellate cells is mediated by a small number of fast-spiking interneurons. J Neurosci 26:1219-1230.
62. Swadlow HA (1989) Efferent neurons and suspected interneurons in S-1 vibrissa cortex of the awake rabbit: receptive fields and axonal properties. J Neurophysiol 62:288-308.
63. Swadlow HA (1995) Influence of VPM afferents on putative inhibitory interneurons in S1 of the awake rabbit: evidence from cross-correlation, microstimulation, and latencies to peripheral sensory stimulation. J Neurophysiol 73:1584-1599.
64. Swadlow HA, Gusev AG (2001) The impact of "bursting" thalamic impulses at a neocortical synapse. Nat Neurosci 4:402-408.
65. White EL (1989) Cortical circuit: synaptic organization of the cerebral cortex-structure, function and theory. Boston: Birkhauser.