State-dependent population coding in primary auditory cortex

Journal of Neuroscience

Volumn 35, Issue 5, 2015, Pages 2058-2073

  Pachitariu, Marius ^a   Lyamzin, Dmitry R ^b,c   Sahani, Maneesh ^a   Lesica, Nicholas A ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

Brain state; Cortex; Noise correlations; Population code

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN FUNCTION; EVOKED AUDITORY RESPONSE; EXPERIMENTAL LOCOMOTOR ACTIVITY TEST; GERBIL; MALE; NEUROPHYSIOLOGY; NEUROSCIENCE; NONHUMAN; PRIMARY AUDITORY CORTEX; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SENSORY CORTEX; SENSORY NERVE CONDUCTION; SIGNAL PROCESSING; SPEECH PERCEPTION; SPIKE WAVE; STIMULUS RESPONSE; ANIMAL; AUDITORY CORTEX; CORTICAL SYNCHRONIZATION; CYTOLOGY; NERVE CELL; PHYSIOLOGY;

ANIMALS; AUDITORY CORTEX; CORTICAL SYNCHRONIZATION; EVOKED POTENTIALS, AUDITORY; GERBILLINAE; MALE; NEURONS;

EID: 84922353570     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3318-14.2015     Document Type: Article

References (62)

1. Aizenberg M, Geffen MN (2013) Bidirectional effects of aversive learning on perceptual acuity are mediated by the sensory cortex. Nat Neurosci 16:994–996. CrossRef Medline
2. 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
3. Azouz R, Gray CM (2003) Adaptive coincidence detection and dynamic gain control in visual cortical neurons in vivo. Neuron 37:513–523. CrossRef Medline
4. Banerjee SB, Liu RC (2013) Storing maternal memories: hypothesizing an interaction of experience and estrogen on sensory cortical plasticity to learn infant cues. Front Neuroendocrinol 34:300–314. CrossRef Medline
5. Bao S, Chang EF, Woods J, Merzenich MM (2004) Temporal plasticity in the primary auditory cortex induced by operant perceptual learning. Nat Neurosci 7:974–981. CrossRef Medline
6. Bathellier B, Ushakova L, Rumpel S (2012) Discrete neocortical dynamics predict behavioral categorization of sounds. Neuron 76:435–449. CrossRef Medline
7. Bermudez Contreras EJ, Schjetnan AG, Muhammad A, Bartho P, Mc-Naughton BL, Kolb B, Gruber AJ, Luczak A (2013) Formation and reverberation of sequential neural activity patterns evoked by sensory stimulation are enhanced during cortical desynchronization. Neuron 79: 555–566. CrossRef Medline
8. Brenner N, Strong SP, Koberle R, Bialek W, de Ruyter van Steveninck RR (2000) Synergy in a neural code. Neural Comput 12:1531–1552. CrossRef Medline
9. Castro-Alamancos MA (2004a) Dynamics of sensory thalamocortical syn-aptic networks during information processing states. Prog Neurobiol 74: 213–247. CrossRef Medline
10. Castro-Alamancos MA (2004b) Absence of rapid sensory adaptation in neocortex during information processing states. Neuron 41:455–464. CrossRef Medline
11. Castro-AlamancosMA (2009) Corticalupand activated states: implications for sensory information processing. Neurosci:625–634.
12. Castro-Alamancos MA, Gulati T (2014) Neuromodulators produce distinct activated states in neocortex. J Neurosci 34:12353–12367. CrossRef Medline
13. Choi JH, Jung HK, Kim T (2006) A new action potential detector using the MTEO and its effects on spike sorting systems at low signal-to-noise ratios. IEEE Trans Biomed Eng 53:738–746. CrossRef Medline
14. Cooke JE, Zhang H, Kelly JB (2007) Detection of sinusoidal amplitude modulated sounds: deficits after bilateral lesions of auditory cortex in the rat. Hear Res 231:90–99. CrossRef Medline
15. Crochet S, Petersen CC (2006) Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nat Neurosci 9:608–610. CrossRef Medline
16. Curto C, Sakata S,Marguet S, ItskovV,HarrisKD (2009) A simple model of cortical dynamics explains variability and state dependence of sensory responses in urethane-anesthetized auditory cortex. J Neurosci 29: 10600–10612. CrossRef Medline
17. Destexhe A, Hughes SW, Rudolph M, Crunelli V (2007) Are corticotha-lamic “up” states fragmentsofwakefulness? Trends Neurosci 30:334–342. CrossRef Medline
18. Garcia-Lazaro JA, Belliveau LA, Lesica NA (2013) Independent population coding of speech with sub-millisecond precision. J Neurosci 33:19362–19372. CrossRef Medline
19. Giraud AL, Poeppel D (2012) Cortical oscillations and speech processing: emerging computational principles and operations. Nat Neurosci 15: 511–517. CrossRef Medline
20. Goard M, Dan Y (2009) Basal forebrain activation enhances cortical coding of natural scenes. Nat Neurosci 12:1444–1449. CrossRef Medline
21. Greenberg DS, Houweling AR, Kerr JN (2008) Population imaging of ongoing neuronal activity in the visual cortex of awake rats. Nat Neurosci 11:749–751. CrossRef Medline
22. Guo W, Chambers AR, Darrow KN, Hancock KE, Shinn-Cunningham BG, Polley DB (2012) Robustness of cortical topography across fields, laminae, anesthetic states, and neurophysiological signal types. J Neurosci 32:9159–9172. CrossRef Medline
23. Haider B, McCormick DA (2009) Rapid neocortical dynamics: cellular and network mechanisms. Neuron 62:171–189. CrossRef Medline
24. Happel MF, Jeschke M, Ohl FW (2010) Spectral integration in primary auditory cortex attributable to temporally precise convergence of thalamo-cortical and intracortical input. J Neurosci 30:11114–11127. CrossRef Medline
25. Harris KD, Thiele A (2011) Cortical state and attention. Nat Rev Neurosci 12:509–523. CrossRef Medline
26. Hasenstaub A, Sachdev RN, McCormick DA (2007) State changes rapidly modulate cortical neuronal responsiveness. J Neurosci 27:9607–9622. CrossRef Medline
27. Hazan L, Zugaro M, Buzsáki G (2006) Klusters, NeuroScope, NDManager: a free software suite for neurophysiological data processing and visualization. J Neurosci Methods 155:207–216. CrossRef Medline
28. Hirata A, Castro-Alamancos MA (2011) Effects of cortical activation on sensory responses in barrel cortex. J Neurophysiol 105:1495–1505. CrossRef Medline
29. Horvath D, Lesica NA (2011) The effects of interaural time difference and intensity on the coding of low-frequency sounds in the mammalian mid-brain. J Neurosci 31:3821–3827. CrossRef Medline
30. Kayser C, Montemurro MA, Logothetis NK, Panzeri S (2009) Spike-phase coding boosts and stabilizes information carried by spatial and temporal spike patterns. Neuron 61:597–608. CrossRef Medline
31. Lakatos P, Musacchia G, O’connel MN, Falchier AY, Javitt DC, Schroeder CE (2013) The spectrotemporal filter mechanism ofauditory selective attention. Neuron 77:750–761. CrossRef Medline
32. Luczak A, Bartho´ P, Marguet SL, Buzsáki G, Harris KD (2007) Sequential structure of neocortical spontaneous activity in vivo. Proc Natl Acad Sci U S A 104:347–352. CrossRef Medline
33. Luczak A, Barthó P, Harris KD (2009) Spontaneous events outline the realm of possible sensory responses in neocortical populations. Neuron 62:413–425. CrossRef Medline
34. Luczak A, Bartho P, Harris KD (2013) Gating of sensory input by spontaneous cortical activity. J Neurosci 33:1684–1695. CrossRef Medline
35. MacLean JN, Watson BO, Aaron GB, Yuste R (2005) Internal dynamics determine the cortical response to thalamic stimulation. Neuron 48:811–823. CrossRef Medline
36. Magri C, Whittingstall K, Singh V, Logothetis NK, Panzeri S (2009) A toolbox for the fast information analysis of multiple-site LFP, EEG and spike train recordings. BMC Neurosci 10:81. CrossRef Medline
37. Marguet SL, Harris KD (2011) State-dependent representation of amplitude-modulated noise stimuli in rat auditory cortex. J Neurosci 31:6414–6420. CrossRef Medline
38. Niell CM, Stryker MP (2010) Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65:472–479. CrossRef Medline
39. Okun M, Yger P, Marguet SL, Gerard-Mercier F, Benucci A, Katzner S, Busse L, Carandini M, Harris KD (2012) Population rate dynamics and multi-neuron firing patterns in sensory cortex. J Neurosci 32:17108–17119. CrossRef Medline
40. Otazu GH, Tai LH, Yang Y, Zador AM (2009) Engaging in an auditory task suppresses responses in auditory cortex. Nat Neurosci 12:646–654. CrossRef Medline
41. Panzeri S, Senatore R, Montemurro MA, Petersen RS (2007) Correcting for the sampling bias problem in spike train information measures. J Neuro-physiol 98:1064–1072. CrossRef Medline
42. Polack PO, Friedman J, Golshani P (2013) Cellular mechanisms of brain state-dependent gain modulation in visual cortex. Nat Neurosci 16:1331–1339. CrossRef Medline
43. Porter BA, Rosenthal TR, Ranasinghe KG, Kilgard MP (2011) Discrimina-tionofbrief speech sounds is impairedinrats with auditory cortex lesions. Behav Brain Res 219:68–74. CrossRef Medline
44. Poulet JFA, Petersen CC (2008) Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 454:881–885. CrossRef Medline
45. Reed A, Riley J, Carraway R, Carrasco A, Perez C, Jakkamsetti V, Kilgard MP (2011) Cortical map plasticity improves learning but is not necessary for improved performance. Neuron 70:121–131. CrossRef Medline
46. Renart A, de la Rocha J, Bartho P, Hollender L, Parga N, Reyes A, Harris KD (2010) The asynchronous state in cortical circuits. Science 327:587–590. CrossRef Medline
47. Rigas P, Castro-Alamancos MA (2007) Thalamocortical up states: differential effects of intrinsic and extrinsic cortical inputs on persistent activity. J Neurosci 27:4261–4272. CrossRef Medline
48. Ringach DL (2009) Spontaneous and driven cortical activity: implications for computation. Curr Opin Neurobiol 19:439–444. CrossRef Medline
49. Rybalko N, Suta D, Nwabueze-Ogbo F, Syka J (2006) Effect of auditory cortex lesions on the discrimination of frequency-modulated tones in rats. Eur J Neurosci 23:1614–1622. CrossRef Medline
50. Sachidhanandam S, Sreenivasan V, Kyriakatos A, Kremer Y, Petersen CC (2013) Membrane potential correlates of sensory perception in mouse barrel cortex. Nat Neurosci 16:1671–1677. CrossRef Medline
51. Sahani M, Linden J (2003) How linear are auditory cortical responses? In: Advances in neural information processing systems 15 (Becker S, Thrun S, Obermayer K, eds), pp 301–308. Cambridge, MA: MIT.
52. Schmitzer-Torbert N, Jackson J, Henze D, Harris K, Redish AD (2005) Quantitative measures of cluster quality for use in extracellular recordings. Neuroscience 131:1–11. CrossRef Medline
53. Schneider DM, Nelson A, Mooney R (2014) A synaptic and circuit basis for corollary discharge in the auditory cortex. Nature 513:189–194. CrossRef Medline
54. Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85:1969–1985. Medline
55. Strong S, Koberle R, de Ruyter Van Steveninck R, Bialek W (1998) Entropy and information in neural spike trains. Phys Rev Lett 80:197–200. CrossRef
56. Tan AY, Chen Y, Scholl B, Seidemann E, Priebe NJ (2014) Sensory stimulation shifts visual cortex from synchronous to asynchronous states. Nature 509:226–229. CrossRef Medline
57. Ter-Mikaelian M, Sanes DH, Semple MN (2007) Transformation oftempo-ral properties between auditory midbrain and cortex in the awake Mongolian gerbil. J Neurosci 27:6091–6102. CrossRef Medline
58. Thomas H, Tillein J, Heil P, Scheich H (1993) Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus): I. Elec-trophysiological mapping of frequency representation and distinction of fields. Eur J Neurosci 5:882–897. CrossRef Medline
59. Wetzel W, Ohl FW, Wagner T, Scheich H (1998) Right auditory cortex lesion in Mongolian gerbils impairs discrimination of rising and falling frequency-modulated tones. Neurosci Lett 252:115–118. CrossRef Medline
60. Xu S, Jiang W, Poo MM, Dan Y (2012) Activity recall in a visual cortical ensemble. Nat Neurosci 15:449–455:S1–2. CrossRef Medline
61. Zhou M, Liang F, Xiong XR, Li L, Li H, Xiao Z, Tao HW, Zhang LI (2014) Scaling down of balanced excitation and inhibition by active behavioral states in auditory cortex. Nat Neurosci 17:841–850. CrossRef Medline
62. Zion Golumbic EM, Ding N, Bickel S, Lakatos P, Schevon CA, McKhann GM, Goodman RR, Emerson R, Mehta AD, Simon JZ, Poeppel D, Schroeder CE (2013) Mechanisms underlying selective neuronal tracking of attended speech at a “cocktail party.” Neuron 77:980–991. CrossRef Medline