Cited by 179Neural dynamics and brain functionMemory and Neural MechanismsSleep and Wakefulness Research

Breathing coordinates cortico-hippocampal dynamics in mice during offline states

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Karalis, Nikolaos, Sirota, Anton·2022·Nature Communications

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Abstract

Network dynamics have been proposed as a mechanistic substrate for the information transfer across cortical and hippocampal circuits. However, little is known about the mechanisms that synchronize and coordinate these processes across widespread brain regions during offline states. Here we address the hypothesis that breathing acts as an oscillatory pacemaker, persistently coupling distributed brain circuit dynamics. Using large-scale recordings from a number of cortical and subcortical brain regions in behaving mice, we uncover the presence of an intracerebral respiratory corollary discharge, that modulates neural activity across these circuits. During offline states, the respiratory modulation underlies the coupling of hippocampal sharp-wave ripples and cortical DOWN/UP state transitions, which mediates systems memory consolidation. These results highlight breathing, a perennial brain rhythm, as an oscillatory scaffold for the functional coordination of the limbic circuit that supports the segregation and integration of information flow across neuronal networks during offline states.

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  • Respiration is also coupled to neural activity in the visual system and influences visual performance.

    “Third, respiration is also coupled to neural activity in the visual system 128,141,146 and influences visual performance 140,146,147 .”

    From Interoceptive rhythms in the brain (2023) · cites this paper as [128]

    The Results section, “Widespread respiratory modulation of limbic circuits during offline states” (page not specified), reports that visual-cortex activity in mice was coupled to breathing. The paper also describes breathing-phase modulation of visually evoked cortical responses, but the passages do not establish an effect on visual performance. (LLM, conf=0.88)

    Experimental — accuracy not yet measured
  • Experimentally, there are only few studies detailing whether different brain regions are coupled to a bodily rhythm with the same phase or different ones, and they are not congruent.

    “Experimentally, there are only few studies detailing whether different brain regions are coupled to a bodily rhythm with the same phase or different ones, and they are not congruent:”

    From Interoceptive rhythms in the brain (2023) · cites this paper as [128]

    The Results section (“Widespread respiratory modulation of limbic circuits during offline states”; page not available) examines how activity in multiple brain regions relates to breathing phase and reports that neurons in several regions fire at distinct phases. The paper does not establish that only a few studies have examined this question or that those studies’ findings are incongruent. (LLM, conf=0.80)

    Experimental — accuracy not yet measured
  • The phase alignment of respiratory-driven neural activity seems rather good.

    “the phase alignment of respiratory-driven neural activity seems rather good 128 ,”

    From Interoceptive rhythms in the brain (2023) · cites this paper as [128]

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  1. [1]Morgane PJ Galler JR Mokler DJ A review of systems and networks of the limbic forebrain/limbic midbrain Prog. Neurobiol. 2005 75 143 160 15784304
  2. [2]Squire LR ‘Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans’ Psychol. Rev. 1992 99 195 231 1594723
  3. [3]McGaugh JL Memory - A century of consolidation Science 2000 287 248 251 10634773
  4. [4]Buzsáki G Memory consolidation during sleep: a neurophysiological perspective J. Sleep Res. 1998 7 17 23 9682189
  5. [5]Battaglia, F. P., Benchenane, K., Sirota, A., Pennartz, C. M. A. & Wiener, S. I. The hippocampus: hub of brain network communication for memory. Trends Cogn. Sci.15, 310–318 (2011). 21696996
  6. [6]Buzsáki, G. Rhythms of the Brain (Oxford Univ. Press, 2006).
  7. [7]Sirota A Buzsáki G Interaction between neocortical and hippocampal networks via slow oscillations Thalamus Relat. Syst. 2005 3 245 18185848 PMC2180396
  8. [8]Buzsaki G Theta oscillations in the hippocampus Neuron 2002 33 325 340 11832222
  9. [10]Buzsáki G Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning Hippocampus 2015 25 1073 1188 26135716 PMC4648295
  10. [11]Sirota A Csicsvari J Buhl DL Buzsaki G Communication between neocortex and hippocampus during sleep in rodents Proc. Natl Acad. Sci. USA 2003 100 2065 2069 12576550 PMC149959
  11. [12]Isomura Y Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations Neuron 2006 52 871 882 17145507
  12. [13]Peyrache A Khamassi M Benchenane K Wiener SI Battaglia FP Replay of rule-learning related neural patterns in the prefrontal cortex during sleep Nat. Neurosci. 2009 12 919 926 19483687
  13. [14]Girardeau G Inema I Buzsáki G Reactivations of emotional memory in the hippocampus–amygdala system during sleep Nat. Neurosci. 2017 20 1634 1642 28892057
  14. [15]Pennartz CMA Ito R Verschure PFMJ Battaglia FP Robbins TW The hippocampal-striatal axis in learning, prediction and goal-directed behavior Trends Neurosci. 2011 34 548 559 21889806
  15. [18]O’Neill J Pleydell-Bouverie B Dupret D Csicsvari J Play it again: reactivation of waking experience and memory Trends Neurosci. 2010 33 220 229 20207025
  16. [20]Ji D Wilson MA Coordinated memory replay in the visual cortex and hippocampus during sleep Nat. Neurosci. 2007 10 100 107 17173043
  17. [23]Maingret N Girardeau G Todorova R Goutierre M Zugaro M Hippocampo-cortical coupling mediates memory consolidation during sleep Nat. Neurosci. 2016 19 959 964 27182818
  18. [24]Maviel T Durkin TP Menzaghi F Bontempi B Sites of neocortical reorganization critical for remote spatial memory Science 2004 305 96 99 15232109
  19. [25]Kitamura T Engrams and circuits crucial for systems consolidation of a memory Science 2017 356 73 78 28386011 PMC5493329
  20. [26]Kumar A Rotter S Aertsen A Spiking activity propagation in neuronal networks: reconciling different perspectives on neural coding Nat. Rev. Neurosci. 2010 11 615 627 20725095
  21. [27]Fischer I Zero-lag long-range synchronization via dynamical relaying Phys. Rev. Lett. 2006 97 123902 123902 17025966
  22. [28]Buzsaki G Logothetis NK Singer W Scaling brain size, keeping timing: evolutionary preservation of brain rhythms Neuron 2013 80 751 764 24183025 PMC4009705
  23. [29]Ottoson D Analysis of the electrical activity of the olfactory epithelium Acta Physiol. Scand. Suppl. 1955 35 1 83 13301864
  24. [30]Karalis N 4-Hz oscillations synchronize prefrontal-amygdala circuits during fear behavior Nat. Neurosci. 2016 19 605 612 26878674 PMC4843971
  25. [31]Moberly, A. H. et al. Olfactory inputs modulate respiration-related rhythmic activity in the prefrontal cortex and freezing behavior. Nat. Commun.9, 1528 (2018). PMC5906445 29670106
  26. [32]Yanovsky Y Ciatipis M Draguhn A Tort ABL & Branka, K, J. Slow oscillations in the mouse hippocampus entrained by nasal respiration J. Neurosci. 2014 34 5949 5964 24760854 PMC6608283
  27. [33]Biskamp J Bartos M Sauer JF Organization of prefrontal network activity by respiration-related oscillations Sci. Rep. 2017 7 45508 45508 28349959 PMC5368652
  28. [34]Steriade M Contreras D Curró Dossi R Nuñez A The slow (< 1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks J. Neurosci. 1993 13 3284 3299 8340808 PMC6576531
  29. [35]Bartho P Characterization of neocortical principal cells and interneurons by network interactions and extracellular features J. Neurophysiol. 2004 92 600 608 15056678
  30. [36]Hoover WB Vertes RP Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat Brain Struct. Funct. 2007 212 149 179 17717690
  31. [37]Herry C Johansen JP Encoding of fear learning and memory in distributed neuronal circuits Nat. Neurosci. 2014 17 1644 1654 25413091
  32. [38]Adrian ED Olfactory reactions in the brain of the hedgehog J. Physiol. 1942 100 459 473 16991539 PMC1393326
  33. [39]Macrides F Chorover SL Olfactory bulb units: activity correlated with inhalation cycles and odor quality Science 1972 175 84 87 5008584
  34. [40]Fukunaga I Herb JT Kollo M Boyden ES Schaefer AT Independent control of gamma and theta activity by distinct interneuron networks in the olfactory bulb Nat. Neurosci. 2014 17 1208 1216 24997762 PMC4146518
  35. [41]Rojas-Líbano D Frederick DE Egaña JI Kay LM The olfactory bulb theta rhythm follows all frequencies of diaphragmatic respiration in the freely behaving rat Front. Behav. Neurosci. 2014 8 214 24966821 PMC4053074
  36. [42]Ackels, T., Jordan, R., Schaefer, A. T. & Fukunaga, I. Respiration-locking of olfactory receptor and projection neurons in the mouse olfactory bulb and its modulation by brain state. Front. Cell. Neurosci. 14, 220 (2020). PMC7378796 32765224
  37. [44]Buzsáki G Neural syntax: cell assemblies, synapsembles, and readers Neuron 2010 68 362 385 21040841 PMC3005627
  38. [47]Vanderwolf CH Hippocampal activity, olfaction, and sniffing: an olfactory input to the dentate gyrus Brain Res. 1992 593 197 208 1450928
  39. [48]Nguyen Chi V Hippocampal respiration-driven rhythm distinct from theta oscillations in awake mice J. Neurosci. 2016 36 162 177 26740658 PMC6601786
  40. [49]Lockmann ALV Laplagne DA Leão RN Tort ABL A respiration-coupled rhythm in the rat hippocampus independent of theta and slow oscillations J. Neurosci. 2016 36 5338 5352 27170130 PMC6601803
  41. [50]Valero M Determinants of different deep and superficial CA1 pyramidal cell dynamics during sharp-wave ripples Nat. Neurosci. 2015 18 1281 1290 26214372 PMC4820637
  42. [51]Mizuseki K Diba K Pastalkova E Buzsaki G Hippocampal CA1 pyramidal cells form functionally distinct sublayers Nat. Neurosci. 2011 14 1174 1183 21822270 PMC3164922
  43. [52]Bragin A Jando G Nadasdy Z van Landeghem M Buzsaki G Dentate EEG spikes and associated interneuronal population bursts in the hippocampal hilar region of the rat J. Neurophysiol. 1995 73 1691 1705 7643175
  44. [53]Buzsáki G Hippocampal network patterns of activity in the mouse Neuroscience 2003 116 201 211 12535953
  45. [54]Hargreaves EL Rao G Lee I Knierim JJ Major dissociation between medial and lateral entorhinal input to dorsal hippocampus Science 2005 308 1792 1794 15961670
  46. [55]Henriksen EJ Spatial representation along the proximodistal axis of CA1 Neuron 2010 68 127 137 20920796 PMC3093538
  47. [56]Fernández-Ruiz A Long-duration hippocampal sharp wave ripples improve memory Science 2019 364 1082 1086 31197012 PMC6693581
  48. [57]Sirota A Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm Neuron 2008 60 683 697 19038224 PMC2640228
  49. [58]Stujenske JM Likhtik E Topiwala MA Gordon JA Fear and safety engage competing patterns of theta-gamma coupling in the basolateral amygdala Neuron 2014 83 919 933 25144877 PMC4141236
  50. [59]Adrian ED The electrical activity of the mammalian olfactory bulb Electroencephalogr. Clin. Neurophysiol. 1950 2 377 388 14793507
  51. [60]Freeman JA Nicholson C Experimental optimization of current source-density technique for anuran cerebellum J. Neurophysiol. 1975 38 369 382 165272
  52. [61]Lepousez G Lledo P-M Odor discrimination requires proper olfactory fast oscillations in awake mice Neuron 2013 80 1010 1024 24139818
  53. [62]Leitner FC Spatially segregated feedforward and feedback neurons support differential odor processing in the lateral entorhinal cortex Nat. Neurosci. 2016 19 935 944 27182817
  54. [64]Tort ABL Parallel detection of theta and respiration-coupled oscillations throughout the mouse brain Sci. Rep. 2018 8 1 14 29691421 PMC5915406
  55. [65]Bergman U Ostergren A Gustafson A-L Brittebo B Differential effects of olfactory toxicants on olfactory regeneration Arch. Toxicol. 2002 76 104 112 11914780
  56. [66]Mofleh R Kocsis B Delta-range coupling between prefrontal cortex and hippocampus supported by respiratory rhythmic input from the olfactory bulb in freely behaving rats Sci. Rep. 2021 11 8100 33854115 PMC8046996
  57. [67]Girin B The deep and slow breathing characterizing rest favors brain respiratory-drive Sci. Rep. 2021 11 7044 33782487 PMC8007577
  58. [68]Liu Y McAfee SS Heck DH Hippocampal sharp-wave ripples in awake mice are entrained by respiration Sci. Rep. 2017 7 8950 28827599 PMC5566471
  59. [69]Sullivan D Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: influence of dentate and entorhinal cortical activity J. Neurosci. 2011 31 8605 8616 21653864 PMC3134187
  60. [70]Siapas AG Wilson MA Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep Neuron 1998 21 1123 1128 9856467
  61. [71]Peyrache A Battaglia FP Destexhe A Inhibition recruitment in prefrontal cortex during sleep spindles and gating of hippocampal inputs Proc. Natl Acad. Sci. 2011 108 17207 17212 21949372 PMC3193185
  62. [72]Khodagholy D Gelinas JN Buzsáki G Learning-enhanced coupling between ripple oscillations in association cortices and hippocampus Science 2017 358 369 372 29051381 PMC5872145
  63. [73]Stark E Pyramidal cell-interneuron interactions underlie hippocampal ripple oscillations Neuron 2014 83 467 480 25033186 PMC4393648
  64. [75]Cui Y Defining preBötzinger complex rhythm- and pattern-generating neural microcircuits in vivo Neuron 2016 91 602 614 27497222 PMC4978183
  65. [76]Yackle K Breathing control center neurons that promote arousal in mice Science 2017 355 1411 1415 28360327 PMC5505554
  66. [77]Yang CF Feldman JL Efferent projections of excitatory and inhibitory preBötzinger complex neurons J. Comp. Neurol. 2018 526 1389 1402 29473167 PMC5869167
  67. [78]Yang CF Kim EJ Callaway EM Feldman JL Monosynaptic projections to excitatory and inhibitory preBötzinger complex neurons Front. Neuroanat. 2020 14 58 33013329 PMC7507425
  68. [79]Chang RB Strochlic DE Williams EK Umans BD Liberles SD Vagal sensory neuron subtypes that differentially control breathing Cell 2015 161 622 633 25892222 PMC4842319
  69. [80]Nonomura K Piezo2 senses airway stretch and mediates lung inflation-induced apnoea Nature 2017 541 176 181 28002412 PMC5267560
  70. [81]Crapse TB Sommer MA Corollary discharge across the animal kingdom Nat. Rev. Neurosci. 2008 9 587 600 18641666 PMC5153363
  71. [82]Straka H Simmers J Chagnaud BP A new perspective on predictive motor signaling Curr. Biol. 2018 28 R193 R194 29510116
  72. [83]Shusterman R Smear MC Koulakov AA Rinberg D Precise olfactory responses tile the sniff cycle Nat. Neurosci. 2011 14 1039 1044 21765422 PMC13348895
  73. [84]Jordan R Fukunaga I Kollo M Schaefer AT Active sampling state dynamically enhances olfactory bulb odor representation Neuron 2018 98 1214 1228.e5 29861286 PMC6030445
  74. [85]Moore JD Hierarchy of orofacial rhythms revealed through whisking and breathing Nature 2013 497 205 210 23624373 PMC4159559
  75. [86]Kleinfeld D Deschênes M Wang F Moore JD More than a rhythm of life: breathing as a binder of orofacial sensation Nat. Neurosci. 2014 17 647 651 24762718 PMC4140942
  76. [87]Dejean C Prefrontal neuronal assemblies temporally control fear behaviour Nature 2016 535 420 424 27409809
  77. [88]Jadhav SPP Rothschild G Roumis DKK Frank LMM Coordinated excitation and inhibition of prefrontal ensembles during awake hippocampal sharp-wave ripple events Neuron 2016 90 113 127 26971950 PMC4824654
  78. [89]Acsády L Kamondi A Sík A Freund T Buzsáki G GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus J. Neurosci. 1998 18 3386 3403 9547246 PMC6792657
  79. [90]Shu Y Hasenstaub A McCormick DA Turning on and off recurrent balanced cortical activity Nature 2003 423 288 293 12748642
  80. [91]Timofeev I Grenier F Bazhenov M Sejnowski TJ Steriade M Origin of slow cortical oscillations in deafferented cortical slabs Cerebral Cortex 2000 10 1185 1199 11073868
  81. [92]Sanchez-Vives MV McCormick DA Cellular and network mechanisms of rhytmic recurrent activity in neocortex Nat. Neurosci. 2000 3 1027 1034 11017176
  82. [93]Viczko J Sharma AV Pagliardini S Wolansky T Dickson CT Lack of respiratory coupling with neocortical and hippocampal slow oscillations J. Neurosci. 2014 34 3937 3946 24623771 PMC6705278
  83. [94]Chauvette S Volgushev M Timofeev I Origin of active states in local neocortical networks during slow sleep oscillation Cerebral Cortex 2010 20 2660 2674 20200108 PMC2951844
  84. [96]Lemieux M Chauvette S Timofeev I Neocortical inhibitory activities and long-range afferents contribute to the synchronous onset of silent states of the neocortical slow oscillation J. Neurophysiol. 2015 113 768 779 25392176 PMC4312868
  85. [98]Carr MF Jadhav SP Frank LM Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval Nat. Neurosci. 2011 14 147 153 21270783 PMC3215304
  86. [99]Jadhav SP Kemere C German PW Frank LM Awake hippocampal sharp-wave ripples support spatial memory Science 2012 336 1454 1458 22555434 PMC4441285
  87. [100]Phillips ME Sachdev RNS Willhite DC Shepherd GM Respiration drives network activity and modulates synaptic and circuit processing of lateral inhibition in the olfactory bulb J. Neurosci. 2012 32 85 98 22219272 PMC3566643
  88. [101]Kay LM Freeman WJ Bidirectional processing in the olfactory-limbic axis during olfactory behavior Behav. Neurosci. 1998 112 541 553 9676972
  89. [102]Fontanini A Spano P Bower JM Ketamine–xylazine-induced slow (~1.5 Hz) oscillations in the rat piriform (Olfactory) cortex are functionally correlated with respiration J. Neurosci. 2003 23 7993 8001 12954860 PMC6740491
  90. [103]Zhong W Selective entrainment of gamma subbands by different slow network oscillations Proc. Natl Acad. Sci. 2017 114 4519 4524 28396398 PMC5410835
  91. [104]Courtin J Karalis N Gonzalez-Campo C Wurtz H Herry C Persistence of amygdala gamma oscillations during extinction learning predicts spontaneous fear recovery Neurobiol. Learn. Mem. 2014 113 82 89 24091205
  92. [105]Carmichael JE Gmaz JM van der Meer MAA Gamma oscillations in the rat ventral striatum originate in the piriform cortex J. Neurosci. 2017 37 7962 7974 28716962 PMC6596914
  93. [106]Zelano C Nasal respiration entrains human limbic oscillations and modulates cognitive function J. Neurosci. 2016 36 12448 12467 27927961 PMC5148230
  94. [107]Arzi, A. et al. Humans can learn new information during sleep. Nat. Neurosci.15, 1460–1465 (2012). 22922782
  95. [108]Rasch B Büchel C Gais S Born J Odor cues during slow-wave sleep prompt declarative memory consolidation Science 2007 315 1426 1429 17347444
  96. [109]Perl O Odors enhance slow-wave activity in non-rapid eye movement sleep J. Neurophysiol. 2016 115 2294 2302 26888107 PMC4922455
  97. [110]Brown RP Gerbarg PL Sudarshan Kriya yogic breathing in the treatment of stress, anxiety, and depression: part I—Neurophysiologic model J. Altern. Complement. Med. 2005 11 189 201 15750381
  98. [111]Kunik ME Surprisingly high prevalence of anxiety and depression in chronic breathing disorders Chest 2005 127 1205 1211 15821196
  99. [112]Gold AR Functional somatic syndromes, anxiety disorders and the upper airway: a matter of paradigms Sleep Med. Rev. 2011 15 389 401 21295503
  100. [113]Neuman A Dyspnea in relation to symptoms of anxiety and depression: a prospective population study Resp. Med. 2006 100 1843 1849 16516455
  101. [115]Isosaka T Htr2a-expressing cells in the central amygdala control the hierarchy between innate and learned fear Cell 2015 163 1153 1164 26590419
  102. [116]Lopes, G. et al. Bonsai: an event-based framework for processing and controlling data streams. Front. Neuroinform.9, 7 (2015). PMC4389726 25904861
  103. [117]Yang L Lee K Villagracia J Masmanidis SC Open source silicon microprobes for high throughput neural recording J. Neural Eng. 2020 17 016036 31731284 PMC7227378
  104. [118]Ferguson JE Boldt C Redish AD Creating low-impedance tetrodes by electroplating with additives Sens. Actuators A Phys. 2009 156 388 393 21379404 PMC3048465
  105. [119]Ludwig, K. A. et al. Poly(3,4-ethylenedioxythiophene) (PEDOT) polymer coatings facilitate smaller neural recording electrodes. J. Neural Eng.8, 014001 (2011). PMC3415981 21245527
  106. [120]DiCarlo JJ Lane JW Hsiao SS Johnson KO Marking microelectrode penetrations with fluorescent dyes J. Neurosci. Methods 1996 64 75 81 8869487
  107. [121]Summerlee AJS Paisley AC Goodall CL A method for determining the position of chronically implanted platinum microwire electrodes J. Neurosci. Methods 1982 5 7 11 7057687
  108. [122]Hazan L Zugaro M Buzsaki G Klusters, NeuroScope, NDManager: a free software suite for neurophysiological data processing and visualization J. Neurosci. Methods 2006 155 207 216 16580733
  109. [123]Mitra PP Pesaran B Analysis of dynamic brain imaging data Biophys. J. 1999 76 691 708 9929474 PMC1300074
  110. [124]Masimore B Kakalios J Redish AD Measuring fundamental frequencies in local field potentials J. Neurosci. Methods 2004 138 97 105 15325117
  111. [125]Barnett L Seth AK The MVGC multivariate Granger causality toolbox: a new approach to Granger-causal inference J. Neurosci. Methods 2014 223 50 68 24200508
  112. [127]Siapas AG Lubenov EV Wilson MA Prefrontal phase locking to hippocampal theta oscillations Neuron 2005 46 141 151 15820700
  113. [128]Tort ABL Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task Proc. Natl Acad. Sci. USA 2008 105 20517 20522 19074268 PMC2629291
  114. [129]Pettersen KH Devor A Ulbert I Dale AM Einevoll GT Current-source density estimation based on inversion of electrostatic forward solution: effects of finite extent of neuronal activity and conductivity discontinuities J. Neurosci. Methods 2006 154 116 133 16436298
  115. [130]Ranck JB Specific impedance of rabbit cerebral cortex Exp. Neurol. 1963 7 144 152 13990734
  116. [131]Logothetis NK Kayser C Oeltermann A In vivo measurement of cortical impedance spectrum in monkeys: implications for signal propagation Neuron 2007 55 809 823 17785187
  117. [132]Nicholson C Freeman JA Theory of current source-density analysis and determination of conductivity tensor for anuran cerebellum J. Neurophysiol. 1975 38 356 368 805215
  118. [133]Csicsvari J Massively parallel recording of unit and local field potentials with silicon-based electrodes J. Neurophysiol. 2003 90 1314 1323 12904510
  119. [134]Buzsaki G Lai-Wo SL Vanderwolf CH Cellular bases of hippocampal EEG in the behaving rat Brain Res. Rev. 1983 6 139 171 6357356
  120. [135]Ylinen A Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells Hippocampus 1995 5 78 90 7787949
  121. [136]Senzai Y Buzsáki G Physiological properties and behavioral correlates of hippocampal granule cells and mossy cells Neuron 2017 93 691 704.e5 28132824 PMC5293146
  122. [137]Mitzdorf U Properties of the evoked potential generators: current source-density analysis of visually evoked potentials in the cat cortex Int. J. Neurosci. 1987 33 33 59 3610492
  123. [138]Ray S Maunsell JHR Differences in gamma frequencies across visual cortex restrict their possible use in computation Neuron 2010 67 885 896 20826318 PMC3001273
  124. [139]Senzai Y Fernandez-Ruiz A Buzsáki G Layer-specific physiological features and interlaminar interactions in the primary visual cortex of the mouse Neuron 2019 101 500 513.e5 30635232 PMC6367010
  125. [140]Pachitariu, M., Steinmetz, N., Kadir, S., Carandini, M. & Harris, K. D. Kilosort: realtime spike-sorting for extracellular electrophysiology with hundreds of channels. Preprint at bioRxiv.10.1101/061481 (2016). · DOI
  126. [141]Chung JE A fully automated approach to spike sorting Neuron 2017 95 1381 1394.e6 28910621 PMC5743236
  127. [142]Csicsvari J Hirase H Czurko A Buzsaki G Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat Neuron 1998 21 179 189 9697862
  128. [143]Freund TF Buzsaki G Interneurons of the hippocampus Hippocampus 1996 6 347 470 8915675
  129. [144]Henze DA Intracellular features predicted by extracellular recordings in the hippocampus in vivo J. Neurophysiol. 2000 84 390 400 10899213
  130. [145]Geisler C Brunel N Wang X-J Contributions of intrinsic membrane dynamics to fast network oscillations with irregular neuronal discharges J. Neurophysiol. 2005 94 4344 4361 16093332
  131. [146]Stark E Roux L Eichler R Buzsáki G Local generation of multineuronal spike sequences in the hippocampal CA1 region Proc. Natl Acad. Sci. USA 2015 112 10521 10526 26240336 PMC4547251

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Authors
Karalis, N., & Sirota, A.
Affiliations
Ludwig-Maximilians-Universität München (DE)
Corresponding author
  • Karalis, Nikolaos
  • Sirota, Anton
Venue
Nature Communications
Published
2022-01-24
Volume
13
Issue
1
Pages
467-467
ISSN
2041-1723 (ISSN-L)
OpenAlex
W4207064626
Cited by
179
References
15
Citations by year
2026: 33 · 2025: 39 · 2024: 40 · 2023: 35 · 2022: 32
FWCI
18.82
Type
journal article
Language
en
Open access
Locations
  • Nature Communications (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Open access LMU (Ludwid Maxmilian's Universitat Munchen) (submittedVersion, cc-by)
Funders
  • European Molecular Biology Organization (Long-term fellowship ALTF 914-2018)
  • EC | Horizon 2020 Framework Programme (Marie Skłodowska-Curie grant agreement No. 843236, FETPROACT 723032 (BrainCom))
  • Deutsche Forschungsgemeinschaft (Synergy, Exc1010, SPP 1665, RTG 2175)
  • Bundesministerium für Bildung und Forschung (BCCN Munich 01GQ0440)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
Keywords
breathing, respiratory rhythm, sharp-wave ripples, memory consolidation, corollary discharge, limbic system, neural oscillations
MeSH terms
Memory Consolidation, Animals, Cerebral Cortex, Electrophysiology, Hippocampus, Mice, Inbred C57BL, Respiration, Sleep, Mice

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