Shift in the balance between excitation and inhibition during sensory adaptation of S1 neurons

Journal of Neuroscience

Volumn 28, Issue 49, 2008, Pages 13320-13330

  Heiss, Jaime E ^a   Katz, Yonatan ^a   Ganmor, Elad ^a   Lampl, Ilan ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Barrel cortex; Conductance measurement; Inhibition; Intracellular recordings in vivo; Layer 4; Sensory adaptation

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; EVOKED RESPONSE; EVOKED SOMATOSENSORY RESPONSE; EXCITATION; INTRACELLULAR RECORDING; LATENT PERIOD; NERVE CELL STIMULATION; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SOMATOSENSORY CORTEX; STIMULUS RESPONSE; SYNAPTIC INHIBITION; THALAMUS; VIBRISSA; ACTION POTENTIAL; ADAPTATION; ANIMAL; EXCITATORY POSTSYNAPTIC POTENTIAL; INHIBITORY POSTSYNAPTIC POTENTIAL; MECHANORECEPTOR; NERVE CELL; NERVE CELL INHIBITION; PATCH CLAMP; PERCEPTIVE THRESHOLD; PHYSIOLOGY; SENSORY NERVE; STIMULATION; SYNAPTIC TRANSMISSION; TOUCH; TRIGEMINAL NERVE; WISTAR RAT;

ACTION POTENTIALS; ADAPTATION, PHYSIOLOGICAL; AFFERENT PATHWAYS; ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; INHIBITORY POSTSYNAPTIC POTENTIALS; MECHANORECEPTORS; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; PHYSICAL STIMULATION; RATS; RATS, WISTAR; SENSORY THRESHOLDS; SOMATOSENSORY CORTEX; SYNAPTIC TRANSMISSION; TOUCH; TRIGEMINAL NERVE; VIBRISSAE;

EID: 58149395076     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2646-08.2008     Document Type: Article

References (62)

1. Ahissar E, Sosnik R, Haidarliu S (2000) Transformation from temporal to rate coding in a somatosensory thalamocortical pathway. Nature 406:302-306.
2. Ahissar E, Sosnik R, Bagdasarian K, Haidarliu S (2001) Temporal frequency of whisker movement. II. Laminar organization of cortical representations. J Neurophysiol 86:354-367.
3. Anderson JS, Carandini M, Ferster D (2000) Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J Neurophysiol 84:909-926.
4. Arabzadeh E, Zorzin E, Diamond ME (2005) Neuronal encoding of texture in the whisker sensory pathway. PLoS Biol 3:e17.
5. Beierlein M, Fall CP, Rinzel J, Yuste R (2002) Thalamocortical bursts trigger recurrent activity in neocortical networks: layer 4 as a frequency-dependent gate. J Neurosci 22:9885-9894.
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. Berg RW, Kleinfeld D (2003) Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. J Neurophysiol 89:104-117.
8. Boudreau CE, Ferster D (2005) Short-term depression in thalamocortical synapses of cat primary visual cortex. J Neurosci 25:7179-7190.
9. 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 543:49-70.
10. Brecht M, Roth A, Sakmann B (2003) Dynamic receptive fields of reconstructed pyramidal cells in layers 3 and 2 of rat somatosensory barrel cortex. J Physiol 553:243-265.
11. Bruno RM, Sakmann B (2006) Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312:1622-1627.
12. Bruno RM, Simons DJ (2002) Feedforward mechanisms of excitatory and inhibitory cortical receptive fields. J Neurosci 22:10966-10975.
13. Bruno RM, Khatri V, Land PW, Simons DJ (2003) Thalamocortical angular tuning domains within individual barrels of rat somatosensory cortex. J Neurosci 23:9565-9574.
14. Carandini M, Ferster D (1997) A tonic hyperpolarization underlying contrast adaptation in cat visual cortex. Science 276:949-952.
15. Carvell GE, Simons DJ (1990) Biometric analyses of vibrissal tactile discrimination in the rat. J Neurosci 10:2638-2648.
16. Castro-Alamancos MA (2002) Role of thalamocortical sensory suppression during arousal: focusing sensory inputs in neocortex. J Neurosci 22:9651-9655.
17. Castro-Alamancos MA (2004) Absence of rapid sensory adaptation in neocortex during information processing states. Neuron 41:455-464.
18. Chelaru MI, Dragoi V (2008) Asymmetric synaptic depression in cortical networks. Cereb Cortex 18:771-788.
19. 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.
20. Connors BW, Prince DA (1982) Effects of local anesthetic QX-314 on the membrane properties of hippocampal pyramidal neurons. J Pharmacol Exp Ther 220:476-481.
21. Cowan AI, Stricker C (2004) Functional connectivity in layer IV local excitatory circuits of rat somatosensory cortex. J Neurophysiol 92:2137-2150.
22. Cruikshank SJ, Lewis TJ, Connors BW (2007) Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nat Neurosci 10:462-468.
23. Dealy RS, Tolhurst DJ (1974) Is spatial adaptation an after-effect of prolonged inhibition? J Physiol 241:261-270.
24. Derdikman D, Yu C, Haidarliu S, Bagdasarian K, Arieli A, Ahissar E (2006) Layer-specific touch-dependent facilitation and depression in the somatosensory cortex during active whisking. J Neurosci 26:9538-9547.
25. Douglas RJ, Koch C, Mahowald M, Martin KA, Suarez HH (1995) Recurrent excitation in neocortical circuits. Science 269:981-985.
26. Ego-Stengel V, Mello e Souza T, Jacob V, Shulz DE (2005) Spatiotemporal characteristics of neuronal sensory integration in the barrel cortex of the rat. J Neurophysiol 93:1450-1467.
27. Gabernet L, Jadhav SP, Feldman DE, Carandini M, Scanziani M (2005) Somatosensory integration controlled by dynamic thalamocortical feedforward inhibition. Neuron 48:315-327.
28. Galarreta M, Hestrin S (1998) Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nat Neurosci 1:587-594.
29. Garabedian CE, Jones SR, Merzenich MM, Dale A, Moore CI (2003) Bandpass response properties of rat SI neurons. J Neurophysiol 90:1379-1391.
30. Gil Z, Connors BW, Amitai Y (1999) Efficacy of thalamocortical and intracortical synaptic connections: quanta, innervation, and reliability. Neuron 23:385-397.
31. Hartings JA, Temereanca S, Simons DJ (2003) Processing of periodic whisker deflections by neurons in the ventroposterior medial and thalamic reticular nuclei. J Neurophysiol 90:3087-3094.
32. Hellweg FC, Schultz W, Creutzfeldt OD (1977) Extracellular and intracellular recordings from cat's cortical whisker projection area: thalamocortical response transformation. J Neurophysiol 40:463-479.
33. Higley MJ, Contreras D (2006) Balanced excitation and inhibition determine spike timing during frequency adaptation. J Neurosci 26:448-457.
34. Hirata A, Castro-Alamancos MA (2008) Cortical transformation of wide-field (multiwhisker) sensory responses. J Neurophysiol 100:358-370.
35. Katz Y, Heiss JE, Lampl I (2006) Cross-whisker adaptation of neurons in the rat barrel cortex. J Neurosci 26:13363-13372.
36. Khatri V, Simons DJ (2007) Angularly nonspecific response suppression in rat barrel cortex. Cereb Cortex 17:599-609.
37. Khatri V, Hartings JA, Simons DJ (2004) Adaptation in thalamic barreloid and cortical barrel neurons to periodic whisker deflections varying in frequency and velocity. J Neurophysiol 92:3244-3254.
38. Knutsen PM, Pietr M, Ahissar E (2006) Haptic object localization in the vibrissal system: behavior and performance. J Neurosci 26:8451-8464.
39. Liu BH, Wu GK, Arbuckle R, Tao HW, Zhang LI (2007) Defining cortical frequency tuning with recurrent excitatory circuitry. Nat Neurosci 10:1594-1600.
40. Lübke J, Egger V, Sakmann B, Feldmeyer D (2000) Columnar organization of dendrites and axons of single and synaptically coupled excitatory spiny neurons in layer 4 of the rat barrel cortex. J Neurosci 20:5300-5311.
41. Maravall M, Petersen RS, Fairhall AL, Arabzadeh E, Diamond ME (2007) Shifts in coding properties and maintenance of information transmission during adaptation in barrel cortex. PLoS Biol 5:e19.
42. Melzer P, Champney GC, Maguire MJ, Ebner FF (2006) Rate code and temporal code for frequency of whisker stimulation in rat primary and secondary somatic sensory cortex. Exp Brain Res 172:370-386.
43. Mittmann W, Koch U, Häusser M (2005) Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells. J Physiol 563:369-378.
44. Nathan T, Jensen MS, Lambert JD (1990) The slow inhibitory postsynaptic potential in rat hippocampal CA1 neurones is blocked by intracellular injection of QX-314. Neurosci Lett 110:309-313.
45. Okun M, Lampl I (2008) Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities. Nat Neurosci 11:535-537.
46. Perkins KL, Wong RK (1995) Intracellular QX-314 blocks the hyperpolarization-activated inward current Iq in hippocampal CA1 pyramidal cells. J Neurophysiol 73:911-915.
47. Petersen CC (2002) Short-term dynamics of synaptic transmission within the excitatory neuronal network of rat layer 4 barrel cortex. J Neurophysiol 87:2904-2914.
48. 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.
49. Priebe NJ, Ferster D (2005) Direction selectivity of excitation and inhibition in simple cells of the cat primary visual cortex. Neuron 45:133-145.
50. Sanchez-Vives MV, Nowak LG, McCormick DA (2000) Membrane mechanisms underlying contrast adaptation in cat area 17 in vivo. J Neurosci 20:4267-4285.
51. Sosnik R, Haidarliu S, Ahissar E (2001) Temporal frequency of whisker movement. I. Representations in brain stem and thalamus. J Neurophysiol 86:339-353.
52. Stratford KJ, Tarczy-Hornoch K, Martin KA, Bannister NJ, Jack JJ (1996) Excitatory synaptic inputs to spiny stellate cells in cat visual cortex. Nature 382:258-261.
53. 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.
54. Swadlow HA (2003) Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. Cereb Cortex 13:25-32.
55. Swadlow HA, Gusev AG (2000) The influence of single VB thalamocortical impulses on barrel columns of rabbit somatosensory cortex. J Neurophysiol 83:2802-2813.
56. Swadlow HA, Gusev AG (2001) The impact of 'bursting' thalamic impulses at a neocortical synapse. Nat Neurosci 4:402-408.
57. Tan AY, Zhang LI, Merzenich MM, Schreiner CE (2004) Tone-evoked excitatory and inhibitory synaptic conductances of primary auditory cortex neurons. J Neurophysiol 92:630-643.
58. Webber RM, Stanley GB (2006) Transient and steady-state dynamics of cortical adaptation. J Neurophysiol 95:2923-2932.
59. Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442-446.
60. Wehr M, Zador AM (2005) Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron 47:437-445.
61. Wilent WB, Contreras D (2005) Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat Neurosci 8:1364-1370.
62. Wu GK, Li P, Tao HW, Zhang LI (2006) Nonmonotonic synaptic excitation and imbalanced inhibition underlying cortical intensity tuning. Neuron 52:705-715.