Postsynaptic mechanisms govern the differential excitation of cortical neurons by thalamic inputs

Journal of Neuroscience

Volumn 29, Issue 28, 2009, Pages 9127-9136

  Hull, Court ^a   Isaacson, Jeffry S ^b   Scanziani, Massimo ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR 2; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; BRAIN CORTEX; BRAIN ELECTROPHYSIOLOGY; CELL TYPE; CONTROLLED STUDY; EVOKED RESPONSE; EXCITATION; FAST SPIKING INTERNEURON; INTERNEURON; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE CELL STIMULATION; NONHUMAN; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; REGULAR SPIKING PRINCIPAL CELL; SENSORY NERVE CELL; SENSORY STIMULATION; SYNAPSE; THALAMUS;

ANIMALS; ANIMALS, NEWBORN; BIOPHYSICS; CALCIUM; DRUG INTERACTIONS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; INHIBITORY POSTSYNAPTIC POTENTIALS; MICE; MICE, INBRED ICR; NEURAL INHIBITION; NEURAL PATHWAYS; NEURONS; PATCH-CLAMP TECHNIQUES; PRINCIPAL COMPONENT ANALYSIS; PYRIDAZINES; RECEPTORS, N-METHYL-D-ASPARTATE; SOMATOSENSORY CORTEX; STRONTIUM; SYNAPSES; THALAMUS; TIME FACTORS;

EID: 67650760005     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5971-08.2009     Document Type: Article

References (56)

1. Agmon A, Connors BW (1991) Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41:365-379.
2. Ahmed B, Anderson JC, Douglas RJ, Martin KA, Nelson JC (1994) Polyneuronal innervation of spiny stellate neurons in cat visual cortex. J Comp Neurol 341:39-49.
3. Angulo MC, Rossier J, Audinat E (1999) Postsynaptic glutamate receptors and integrative properties of fast-spiking interneurons in the rat neocortex. J Neurophysiol 82:1295-1302.
4. Armstrong-James M, Welker E, Callahan CA (1993) The contribution of NMDA and non-NMDA receptors to fast and slow transmission of sensory information in the rat SI barrel cortex. J Neurosci 13:2149 -2160.
5. Beierlein M, Connors BW (2002) Short-term dynamics of thalamocortical and intracortical synapses onto layer 6 neurons in neocortex. J Neurophysiol 88:1924 -1932.
6. Beierlein M, Gibson JR, Connors BW (2003) Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90:2987-3000.
7. Binshtok AM, Fleidervish IA, Sprengel R, Gutnick MJ (2006) NMDAreceptors in layer 4 spiny stellate cells of the mouse barrel cortex contain the NR2C subunit. J Neurosci 26:708 -715.
8. Bochet P, Audinat E, Lambolez B, Crépel F, Rossier J, Iino M, Tsuzuki K, Ozawa S (1994) Subunit composition at the single-cell level explains functional properties of a glutamate-gated channel. Neuron 12:383-388.
9. Brumberg JC, Pinto DJ, Simons DJ (1996) Spatial gradients and inhibitory summation in the rat whisker barrel system. J Neurophysiol 76:130 -140.
10. Bruno RM, Sakmann B (2006) Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312:1622-1627.
11. Clements JD (2003) Variance-mean analysis: a simple and reliable approach for investigating synaptic transmission and modulation. J Neurosci Methods 130:115-125.
12. Clements JD, Silver RA (2000) Unveiling synaptic plasticity: a new graphical and analytical approach. Trends Neurosci 23:105-113.
13. Cruikshank SJ, Lewis TJ, Connors BW (2007) Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nat Neurosci 10:462- 468.
14. Feldmeyer D, Egger V, Lubke J, Sakmann B (1999) Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single 'barrel' of developing rat somatosensory cortex. J Physiol 521:169 -190.
15. Ferster D, Lindström S (1985) Augmenting responses evoked in area 17 of the cat by intracortical axon collaterals of cortico-geniculate cells. J Physiol 367:217-232.
16. Fleidervish IA, Binshtok AM, Gutnick MJ (1998) Functionally distinct NMDAreceptors mediate horizontal connectivity within layer 4 of mouse barrel cortex. Neuron 21:1055-1065.
17. Gabernet L, Jadhav SP, Feldman DE, Carandini M, ScanzianiM (2005) Somatosensory integration controlled by dynamic thalamocortical feedforward inhibition. Neuron 48:315-327.
18. Geiger JR, Melcher T, Koh DS, Sakmann B, Seeburg PH, Jonas P, Monyer H (1995) Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15:193-204.
19. Geiger JR, Lübke J, Roth A, Frotscher M, Jonas P (1997) Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18:1009 -1023.
20. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75-79.
21. Gil Z, Amitai Y (1996) Adult thalamocortical transmission involves both NMDA and non-NMDA receptors. J Neurophysiol 76:2547-2554.
22. Gil Z, Connors BW, Amitai Y (1999) Efficacy of thalamocortical and intracortical synaptic connections: quanta, innervation, and reliability. Neuron 23:385-397.
23. Goda Y, Stevens CF (1994) Two components of transmitter release at a central synapse. Proc Natl Acad Sci U S A 91:12942-12946.
24. Harris RM, Woolsey TA (1983) Computer-assisted analyses of barrel neuron axons and their putative synaptic contacts. JCompNeurol 220:63-79.
25. Higley MJ, Contreras D (2006) Balanced excitation and inhibition determine spike timing during frequency adaptation. J Neurosci 26:448-457.
26. Inoue T, Imoto K (2006) Feedforward inhibitory connections from multiple thalamic cells to multiple regular-spiking cells in layer 4 of the somatosensory cortex. J Neurophysiol 96:1746 -1754.
27. Jonas P, Racca C, Sakmann B, Seeburg PH, MonyerH (1994) Differences in Ca2+ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression. Neuron 12:1281-1289.
28. Kasamatsu T, Imamura K, Mataga N, Hartveit E, Heggelund U, Heggelund P (1998) Roles of N-methyl-D-aspartate receptors in ocular dominance plasticity in developing visual cortex: re-evaluation. Neuroscience 82:687-700.
29. Koh DS, Geiger JR, Jonas P, Sakmann B (1995) Ca(2+)-permeable AMPA and NMDA receptor channels in basket cells of rat hippocampal dentate gyrus. J Physiol 485:383- 402.
30. Kuner T, Schoepfer R (1996) Multiple structural elements determine subunit specificity of Mg2+ block in NMDA receptor channels. J Neurosci 16:3549 -3558.
31. Kyriazi HT, Carvell GE, Simons DJ (1994) OFF response transformations in the whisker/barrel system. J Neurophysiol 72:392- 401.
32. Lamsa KP, Heeroma JH, Somogyi P, Rusakov DA, Kullmann DM (2007) Anti-Hebbian long-term potentiation in the hippocampal feedback inhibitory circuit. Science 315:1262-1266.
33. Ling DS, Benardo LS (1995) Recruitment ofGABAAinhibition in rat neocortex is limited and not NMDA dependent. J Neurophysiol 74:2329-2335.
34. Liu SQ, Cull-Candy SG (2000) Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 405:454-458.
35. McBain CJ, Dingledine R (1993) Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurones of rat hippocampus. J Physiol 462:373-392.
36. McCormick DA, Connors BW, Lighthall JW, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54:782- 806.
37. Miller KD, Chapman B, Stryker MP (1989) Visual responses in adult cat visual cortex depend on N-methyl-D-aspartate receptors. Proc Natl Acad Sci U S A 86:5183-5187.
38. Petersen RS, Panzeri S, Diamond ME (2001) Population coding of stimulus location in rat somatosensory cortex. Neuron 32:503-514.
39. Pinto DJ, Brumberg JC, Simons DJ (2000) Circuit dynamics and coding strategies in rodent somatosensory cortex. J Neurophysiol 83:1158 -1166.
40. Porter JT, Johnson CK, Agmon A (2001) Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex. J Neurosci 21:2699 -2710.
41. Sherman SM, Guillery RW (1996) Functional organization of thalamocortical relays. J Neurophysiol 76:1367-1395.
42. Silver RA (2003) Estimation of nonuniform quantal parameters with multiple-probability fluctuation analysis: theory, application and limitations. J Neurosci Methods 130:127-141.
43. Silver RA,MomiyamaA, Cull-CandySG (1998) Locus of frequency-dependent depression identified with multiple-probability fluctuation analysis at rat climbing fibre-Purkinje cell synapses. J Physiol 510:881-902.
44. Simons DJ (1978) Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophysiol 41:798-820.
45. Simons DJ, Woolsey TA (1984) Morphology of Golgi-Cox-impregnated barrel neurons in rat SmI cortex. J Comp Neurol 230:119 -132.
46. 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.
47. Swadlow HA (2003) Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. Cereb Cortex 13:25-32.
48. Swadlow HA, Gusev AG (2000) The influence of single VB thalamocortical impulses on barrel columns of rabbit somatosensory cortex. J Neurophysiol 83:2802-2813.
49. Swadlow HA, Gusev AG (2002) Receptive-field construction in cortical inhibitory interneurons. Nat Neurosci 5:403- 404.
50. Swanson GT, Kamboj SK, Cull-Candy SG (1997) Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J Neurosci 17:58-69.
51. Wang Y, Gupta A, Toledo-Rodriguez M, Wu CZ, Markram H (2002) Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. Cereb Cortex 12:395- 410.
52. Wehr M, ZadorAM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442- 446.
53. White EL, Rock MP (1980) Three-dimensional aspects and synaptic relationships of a Golgi-impregnated spiny stellate cell reconstructed from serial thin sections. J Neurocytol 9:615- 636.
54. Wilent WB, Contreras D (2004) Synaptic responses to whisker deflections in rat barrel cortex as a function of cortical layer and stimulus intensity. J Neurosci 24:3985-3998.
55. Wilent WB, Contreras D (2005) Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat Neurosci 8:1364 -1370.
56. Zhang ZW, Deschênes M (1998) Projections to layer VI of the posteromedial barrel field in the rat: a reappraisal of the role of corticothalamic pathways. Cereb Cortex 8:428-436.