Gain modulation of synaptic inputs by network state in auditory cortex in vivo

Journal of Neuroscience

Volumn 35, Issue 6, 2015, Pages 2689-2702

  Reig, Ramon ^a,d   Zerlaut, Yann ^b   Vergara, Ramiro ^a,e   Destexhe, Alain ^b   Sanchez Vives, Maria V ^a,c  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b CNRS   (France)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^d KAROLINSKA INSTITUTE   (Sweden)

^e UNIVERSIDAD NACIONAL DE QUILMES   (Argentina)

Author keywords

Cerebral cortex; Computational model; Oscillations; Synaptic inputs; Thalamocortical; Up states

Indexed keywords

ACTION POTENTIAL; ADULT; ANESTHESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; BRAIN DEPTH STIMULATION; COMPUTER ANALYSIS; ELECTROENCEPHALOGRAM; ELECTROSTIMULATION; EVOKED AUDITORY RESPONSE; EXCITABILITY; IN VIVO STUDY; INTRACELLULAR RECORDING; INTRACORTICAL ELECTRICAL STIMULATION; MALE; MATHEMATICAL MODEL; NERVE CELL MEMBRANE CONDUCTANCE; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NETWORK; NERVE STIMULATION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; SLOW WAVE SLEEP; STIMULUS RESPONSE; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; THALAMOCORTICAL ACTIVATION; ANIMAL; BIOLOGICAL MODEL; NERVE CONDUCTION; NERVE TRACT; PHYSIOLOGY; SYNAPSE; THALAMUS; WISTAR RAT;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY CORTEX; ELECTRIC STIMULATION; MALE; MODELS, NEUROLOGICAL; NERVE NET; NEURAL CONDUCTION; NEURAL PATHWAYS; RATS; RATS, WISTAR; SYNAPSES; SYNAPTIC TRANSMISSION; THALAMUS;

EID: 84922572486     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2004-14.2015     Document Type: Article

References (50)

1. Arieli A, Sterkin A, Grinvald A, Aertsen A (1996) Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 273: 1868-1871. CrossRef Medline.
2. Azouz R, Gray CM (1999) Cellular mechanisms contributing to response variability of cortical neurons in vivo. J Neurosci 19: 2209-2223. Medline.
3. Boudreau CE, Ferster D (2005) Short-term depression in thalamocortical synapses of cat primary visual cortex. J Neurosci 25: 7179-7190. CrossRef Medline.
4. Castro-Alamancos MA (2002) Different temporal processing of sensory inputs in the rat thalamus during quiescent and information processing states in vivo. J Physiol 539: 567-578. CrossRef Medline.
5. Castro-Alamancos MA, Oldford E (2002) Cortical sensory suppression during arousal is due to the activity-dependent depression of thalamocortical synapses. J Physiol 541: 319-331. CrossRef Medline.
6. Compte A, Reig R, Sanchez-Vives M (2009) Timing excitation and inhibition in the cortical network. In: Coherent behavior in neuronal networks (Josic K, Rubin J, Matias M, Romo R, eds), pp 17-46. New York: Springer.
7. Constantinople CM, BrunoRM (2011) Effects and mechanisms of wakefulness on local cortical networks. Neuron 69: 1061-1068. CrossRef Medline.
8. Contreras D, Timofeev I, Steriade M (1996) Mechanisms of long-lasting hyperpolarizations underlying slow sleep oscillations in cat corticothalamic networks. J Physiol 494: 251-264. CrossRef Medline.
9. 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. Medline.
10. Crochet S, Chauvette S, Boucetta S, Timofeev I (2005) Modulation of synaptic transmission in neocortex by network activities. Eur J Neurosci 21: 1030-1044. CrossRef Medline.
11. Crochet S, Fuentealba P, Cissé Y, Timofeev I, Steriade M (2006) Synaptic plasticity in local cortical network in vivo and its modulation by the level of neuronal activity. Cereb Cortex 16: 618-631. Medline.
12. Deco G, Martí D, Ledberg A, Reig R, Vives MVS (2009) Effective reduced diffusion-models: a data driven approach to the analysis of neuronal dynamics. PLoS Comput Biol 5: e1000587. CrossRef Medline.
13. Destexhe A (2009) Self-sustained asynchronous irregular states and Up-Down states in thalamic, cortical and thalamocortical networks of nonlinear integrate-and-fire neurons. J Comput Neurosci 27: 493-506. CrossRef Medline.
14. Destexhe A, Contreras D (2006) Neuronal computations with stochastic network states. Science 314: 85-90. CrossRef Medline.
15. Destexhe A, Hughes SW, Rudolph M, Crunelli V (2007) Are corticothalamic 'up' states fragments of wakefulness? Trends Neurosci 30: 334-342. CrossRef Medline.
16. Gil Z, Amitai Y (1996) Properties of convergent thalamocortical and intracortical synaptic potentials in single neurons of neocortex. J Neurosci 16: 6567-6578. Medline.
17. Haider B, Duque A, Hasenstaub AR, Yu Y, McCormick DA (2007) Enhancement of visual responsiveness by spontaneous local network activity in vivo. J Neurophysiol 97: 4186-4202. CrossRef Medline.
18. Hasenstaub A, Sachdev RN, McCormick DA (2007) State changes rapidly modulate cortical neuronal responsiveness. J Neurosci 27: 9607-9622. CrossRef Medline.
19. Hô N, Destexhe A (2000) Synaptic background activity enhances the responsiveness of neocortical pyramidal neurons. J Neurophysiol 84: 1488-1496. Medline.
20. Hromádka T, Zador AM, DeWeese MR (2013) Up states are rare in awake auditory cortex. J Neurophysiol 109: 1989-1995. CrossRef Medline.
21. Kuhn A, Aertsen A, Rotter S (2004) Neuronal integration of synaptic input in the fluctuation-driven regime. J Neurosci 24: 2345-2356. Medline.
22. Lapicque L (1907) Recherches quantitatives sur l'excitation électrique des nerfs traitée comme une polarisation. J Physiol Pathol Gen 9: 620-635.
23. Logothetis NK, Kayser C, Oeltermann A (2007) In vivo measurement of cortical impedance spectrum in monkeys: implications for signal propagation. Neuron 55: 809-823. CrossRef Medline.
24. Lorente de No R (1938) Analysis of the activity of the chains of internuncial neurons. J Neurophysiol 1: 207-244.
25. Luczak A, Barthó P, HarrisKD (2009) Spontaneous events outline the realm of possible sensory responses in neocortical populations. Neuron 62: 413-425. CrossRef Medline.
26. 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. Medline.
27. Nowak LG, Sanchez-Vives MV, McCormick DA (1997) Influence of low and high frequency inputs on spike timing in visual cortical neurons. Cereb Cortex 7: 487-501. CrossRef Medline.
28. Nowak LG, Azouz R, Sanchez-Vives MV, Gray CM, McCormick DA (2003) Electrophysiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses. J Neurophysiol 89: 1541-1566. Medline.
29. Paré D, Shink E, Gaudreau H, Destexhe A, Lang EJ (1998) Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons in vivo. J Neurophysiol 79: 1450-1460. Medline.
30. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates, ed 5. Amsterdam: Elsevier Academic.
31. 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 U S A 100: 13638-13643. CrossRef Medline.
32. Ranck JB Jr (1975) Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 98: 417-440. CrossRef Medline.
33. Rees A, Sarbaz A, Malmierca MS, Le Beau FE (1997) Regularity of firing of neurons in the inferior colliculus. J Neurophysiol 77: 2945-2965. Medline.
34. Reig R, Sanchez-VivesMV (2007) Synaptic transmission and plasticity in an active cortical network. PLoS One 2: e670. CrossRef Medline.
35. Reig R, Gallego R, Nowak LG, Sanchez-Vives MV (2006) Impact of cortical network activity on short-term synaptic depression. Cereb Cortex 16: 688-695. CrossRef Medline.
36. Richardson MJ (2004) Effects of synaptic conductance on the voltage distribution and firing rate of spiking neurons. Phys Rev E Stat Nonlin Soft Matter Phys 69: 051918. CrossRef Medline.
37. Rigas P, Castro-Alamancos MA (2009) Impact of persistent cortical activity (up States) on intracortical and thalamocortical synaptic inputs. J Neurophysiol 102: 119-131. CrossRef Medline.
38. Rudolph M, Piwkowska Z, Badoual M, Bal T, Destexhe A (2004) A method to estimate synaptic conductances from membrane potential fluctuations. J Neurophysiol 91: 2884-2896. CrossRef Medline.
39. Sachdev RN, Ebner FF, Wilson CJ (2004) Effect of subthreshold up and down states on the whisker-evoked response in somatosensory cortex. J Neurophysiol 92: 3511-3521. CrossRef Medline.
40. Sakata S, Harris KD (2009) Laminar structure of spontaneous and sensoryevoked population activity in auditory cortex. Neuron 64: 404-418. CrossRef Medline.
41. Sanchez-Vives MV, McCormick DA (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3: 1027-1034. CrossRef Medline.
42. Sanchez-Vives MV, Nowak LG, Descalzo VF, Garcia-Velasco JV, Gallego R, Berbel P (2006) Crossmodal audio-visual interactions in the primary visual cortex of the visually deprived cat: a physiological and anatomical study. Prog Brain Res 155: 287-311. CrossRef Medline.
43. Seamari Y, Narváez JA, Vico FJ, Lobo D, Sanchez-Vives MV (2007) Robust off-and online separation of intracellularly recorded up and down cortical states. PLoS One 2: e888. CrossRef Medline.
44. Steriade M (2001) Impact of network activities on neuronal properties in corticothalamic systems. J Neurophysiol 86: 1-39. Medline.
45. Steriade M, Nuñez A, Amzica F (1993) A novel slow (+1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci 13: 3252-3265. Medline.
46. Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85: 1969-1985. Medline.
47. Timofeev I, Contreras D, SteriadeM (1996) Synaptic responsiveness of cortical and thalamic neurones during various phases of slow sleep oscillation in cat. J Physiol 494: 265-278. CrossRef Medline.
48. Waters J, Helmchen F (2006) Background synaptic activity is sparse in neocortex. J Neurosci 26: 8267-8277. CrossRef Medline.
49. Wolfart J, Debay D, Le Masson G, Destexhe A, Bal T (2005) Synaptic background activity controls spike transfer from thalamus to cortex. Nat Neurosci 8: 1760-1767. CrossRef Medline.
50. Zou Q, Rudolph M, Roy N, Sanchez-Vives M, Contreras D, Destexhe A (2005) Reconstructing synaptic background activity from conductance measurements in vivo. Neurocomputing 65: 673-678. CrossRef.