Abstract
The cerebral cortex forms a sheet of neurons organized into a network of interconnected modules that is highly expanded in humans and presumably enables our most refined sensory and cognitive abilities. The links of this network form a fundamental aspect of its organization, and a great deal of research is focusing on understanding how information flows within and between different regions. However, an often-overlooked element of this connectivity regards a causal, hierarchical structure of regions, whereby certain nodes of the cortical network may exert greater influence over the others. While this is difficult to ascertain non-invasively, patients undergoing invasive electrode monitoring for epilepsy provide a unique window into this aspect of cortical organization. In this review, we highlight the potential for cortico-cortical evoked potential (CCEP) mapping to directly measure neuronal propagation across large-scale brain networks with spatio-temporal resolution that is superior to traditional neuroimaging methods. We first introduce effective connectivity and discuss the mechanisms underlying CCEP generation. Next, we highlight how CCEP mapping has begun to provide insight into the neural basis of non-invasive imaging signals. Finally, we present a novel approach to perturbing and measuring brain network function during cognitive processing. The direct measurement of CCEPs in response to electrical stimulation represents a potentially powerful clinical and basic science tool for probing the large-scale networks of the human cerebral cortex.
Footnotes
References
- 1
Raichle ME . 2009 A paradigm shift in functional brain imaging. J. Neurosci. 29, 12 729–12 734. (doi:10.1523/JNEUROSCI.4366-09.2009). Crossref, Web of Science, Google Scholar - 2
Sporns O . 2013 Structure and function of complex brain networks. Dialogues Clin. Neurosci. 15, 247–262. Crossref, PubMed, Google Scholar - 3
- 4
Conturo TE, Lori NF, Cull TS, Akbudak E, Snyder AZ, Shimony JS, McKinstry RC, Burton H& Raichle ME . 1999 Tracking neuronal fiber pathways in the living human brain. Proc. Natl Acad. Sci. USA 96, 10 422–10 427. (doi:10.1073/pnas.96.18.10422). Crossref, Web of Science, Google Scholar - 5
Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ& Sporns O . 2008 Mapping the structural core of human cerebral cortex. PLoS Biol. 6, e159. (doi:10.1371/journal.pbio.0060159). Crossref, PubMed, Web of Science, Google Scholar - 6
Felleman DJ& Van Essen DC . 1991 Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47. (doi:10.1093/cercor/1.1.1). Crossref, PubMed, Web of Science, Google Scholar - 7
Assaf Y& Pasternak O . 2008 Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J. Mol. Neurosci. 34, 51–61. (doi:10.1007/s12031-007-0029-0). Crossref, PubMed, Web of Science, Google Scholar - 8
Mukherjee P, Berman JI, Chung SW, Hess CP& Henry RG . 2008 Diffusion tensor MR imaging and fiber tractography: theoretic underpinnings. Am. J. Neuroradiol. 29, 632–641. (doi:10.3174/ajnr.A1051). Crossref, PubMed, Web of Science, Google Scholar - 9
Honey CJ, Sporns O, Cammoun L, Gigandet X, Thiran JP, Meuli R& Hagmann P . 2009 Predicting human resting-state functional connectivity from structural connectivity. Proc. Natl Acad. Sci. USA 106, 2035–2040. (doi:10.1073/pnas.0811168106). Crossref, PubMed, Web of Science, Google Scholar - 10
van den Heuvel MP, Mandl RC, Kahn RS& Hulshoff Pol HE . 2009 Functionally linked resting-state networks reflect the underlying structural connectivity architecture of the human brain. Hum. Brain Mapp. 30, 3127–3141. (doi:10.1002/hbm.20737). Crossref, PubMed, Web of Science, Google Scholar - 11
Friston KJ . 1994 Functional and effective connectivity in neuroimaging: a synthesis. Hum. Brain Mapp. 2, 56–78. (doi:10.1002/hbm.460020107). Crossref, Google Scholar - 12
Biswal B, Yetkin FZ, Haughton VM& Hyde JS . 1995 Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 34, 537–541. (doi:10.1002/mrm.1910340409). Crossref, PubMed, Web of Science, Google Scholar - 13
Fox MD& Raichle ME . 2007 Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 8, 700–711. (doi:10.1038/nrn2201). Crossref, PubMed, Web of Science, Google Scholar - 14
Friston KJ . 2011 Functional and effective connectivity: a review. Brain Connect. 1, 13–36. (doi:10.1089/brain.2011.0008). Crossref, PubMed, Google Scholar - 15
Aertsen A& Preissl H . 1991 Dynamics of activity and connectivity in physiological neuronal networks. New York, NY: VCH Publishers Inc. Google Scholar - 16
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. (doi:10.1126/science.273.5283.1868). Crossref, PubMed, Web of Science, Google Scholar - 17
Buchel C, Coull JT& Friston KJ . 1999 The predictive value of changes in effective connectivity for human learning. Science 283, 1538–1541. (doi:10.1126/science.283.5407.1538). Crossref, PubMed, Web of Science, Google Scholar - 18
Brovelli A, Ding M, Ledberg A, Chen Y, Nakamura R& Bressler SL . 2004 Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. Proc. Natl Acad. Sci. USA 101, 9849–9854. (doi:10.1073/pnas.0308538101). Crossref, PubMed, Web of Science, Google Scholar - 19
Kayser C& Logothetis NK . 2009 Directed interactions between auditory and superior temporal cortices and their role in sensory integration. Front. Integr. Neurosci. 3, 7. (doi:10.3389/neuro.07.007.2009). Crossref, PubMed, Google Scholar - 20
Kiebel SJ, Garrido MI, Moran R, Chen CC& Friston KJ . 2009 Dynamic causal modeling for EEG and MEG. Hum. Brain Mapp. 30, 1866–1876. (doi:10.1002/hbm.20775). Crossref, PubMed, Web of Science, Google Scholar - 21
Horwitz B . 2003 The elusive concept of brain connectivity. Neuroimage 19, 466–470. (doi:10.1016/S1053-8119(03)00112-5). Crossref, PubMed, Web of Science, Google Scholar - 22
Webb JT, Ferguson MA, Nielsen JA& Anderson JS . 2013 BOLD Granger causality reflects vascular anatomy. PLoS ONE 8, e84279. (doi:10.1371/journal.pone.0084279). Crossref, PubMed, Web of Science, Google Scholar - 23
Ding M, Chen Y& Bressler SL . 2006 Granger causality: basic theory and application to neuroscience. In Handbook of time series analysis, pp. 437–460. Hoboken, NJ: Wiley. Crossref, Google Scholar - 24
Smith SM, Miller KL, Salimi-Khorshidi G, Webster M, Beckmann CF, Nichols TE, Ramsey JD& Woolrich MW . 2011 Network modelling methods for FMRI. Neuroimage 54, 875–891. (doi:10.1016/j.neuroimage.2010.08.063). Crossref, PubMed, Web of Science, Google Scholar - 25
Bullmore E& Sporns O . 2009 Complex brain networks: graph theoretical analysis of structural and functional systems. Nat. Rev. Neurosci. 10, 186–198. (doi:10.1038/nrn2575). Crossref, PubMed, Web of Science, Google Scholar - 26
Beauchamp MS, Sun P, Baum SH, Tolias AS& Yoshor D . 2012 Electrocorticography links human temporoparietal junction to visual perception. Nat. Neurosci. 15, 957–959. (doi:10.1038/nn.3131). Crossref, PubMed, Web of Science, Google Scholar - 27
Suthana N, Haneef Z, Stern J, Mukamel R, Behnke E, Knowlton B& Fried I . 2012 Memory enhancement and deep-brain stimulation of the entorhinal area. N. Engl. J. Med. 366, 502–510. (doi:10.1056/NEJMoa1107212). Crossref, PubMed, Web of Science, Google Scholar - 28
Wessel JR, Conner CR, Aron AR& Tandon N . 2013 Chronometric electrical stimulation of right inferior frontal cortex increases motor braking. J. Neurosci. 33, 19 611–19 619. (doi:10.1523/JNEUROSCI.3468-13.2013). Crossref, Web of Science, Google Scholar - 29
Biswal BB, 2010 Toward discovery science of human brain function. Proc. Natl Acad. Sci. USA 107, 4734–4739. (doi:10.1073/pnas.0911855107). Crossref, PubMed, Web of Science, Google Scholar - 30
Fox MD, Halko MA, Eldaief MC& Pascual-Leone A . 2012 Measuring and manipulating brain connectivity with resting state functional connectivity magnetic resonance imaging (fcMRI) and transcranial magnetic stimulation (TMS). Neuroimage 62, 2232–2243. (doi:10.1016/j.neuroimage.2012.03.035). Crossref, PubMed, Web of Science, Google Scholar - 31
Kobayashi M& Pascual-Leone A . 2003 Transcranial magnetic stimulation in neurology. Lancet Neurol. 2, 145–156. (doi:10.1016/S1474-4422(03)00321-1). Crossref, PubMed, Web of Science, Google Scholar - 32
Vogt O& Vogt C . 1919 Ergebnisse unserer hirnforschung. J. Psychol. Neurol. 25, 279–461. Google Scholar - 33
- 34
Cushing H . 1909 A note upon the faradic stimulation of the postcentral gyrus in conscious patients. Brain 32, 44–53. (doi:10.1093/brain/32.1.44). Crossref, Google Scholar - 35
Foerster O& Altenburger H . 1935 Elektobiologische Vorgänge an der menschlichen Hirnrinde. Dtsche Z. Nervenheilk. 135, 277–288. (doi:10.1007/BF01732786). Crossref, Google Scholar - 36
Penfield W& Boldrey E . 1937 Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60, 389–443. (doi:10.1093/brain/60.4.389). Crossref, Google Scholar - 37
Penfield W& Perot P . 1963 The brain's record of auditory and visual experience. A final summary and discussion. Brain 86, 595–696. (doi:10.1093/brain/86.4.595). Crossref, PubMed, Web of Science, Google Scholar - 38
Purpura DP, Pool J, Frumin M& Housepian E . 1957 Observations on evoked dendritic potentials of human cortex. Electroencephalogr. Clin. Neurophysiol. 9, 453–459. (doi:10.1016/0013-4694(57)90034-2). Crossref, PubMed, Google Scholar - 39
Salzman CD, Britten KH& Newsome WT . 1990 Cortical microstimulation influences perceptual judgements of motion direction. Nature 346, 174–177. (doi:10.1038/346174a0). Crossref, PubMed, Web of Science, Google Scholar - 40
Boyden ES, Zhang F, Bamberg E, Nagel G& Deisseroth K . 2005 Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263–1268. (doi:10.1038/nn1525). Crossref, PubMed, Web of Science, Google Scholar - 41
Desai M, 2011 Mapping brain networks in awake mice using combined optical neural control and fMRI. J. Neurophysiol. 105, 1393–1405. (doi:10.1152/jn.00828.2010). Crossref, PubMed, Web of Science, Google Scholar - 42
Megevand P, Groppe DM, Goldfinger MS, Hwang ST, Kingsley PB, Davidesco I& Mehta AD . 2014 Seeing scenes: topographic visual hallucinations evoked by direct electrical stimulation of the parahippocampal place area. J. Neurosci. 34, 5399–5405. (doi:10.1523/JNEUROSCI.5202-13.2014). Crossref, PubMed, Web of Science, Google Scholar - 43
Parvizi J, Jacques C, Foster BL, Witthoft N, Rangarajan V, Weiner KS& Grill-Spector K . 2012 Electrical stimulation of human fusiform face-selective regions distorts face perception. J. Neurosci. 32, 14 915–14 920. (doi:10.1523/JNEUROSCI.2609-12.2012). Crossref, Web of Science, Google Scholar - 44
Parvizi J, Rangarajan V, Shirer WR, Desai N& Greicius MD . 2013 The will to persevere induced by electrical stimulation of the human cingulate gyrus. Neuron 80, 1359–1367. (doi:10.1016/j.neuron.2013.10.057). Crossref, PubMed, Web of Science, Google Scholar - 45
Hallett M . 2007 Transcranial magnetic stimulation: a primer. Neuron 55, 187–199. (doi:10.1016/j.neuron.2007.06.026). Crossref, PubMed, Web of Science, Google Scholar - 46
Fritsch B, Reis J, Martinowich K, Schambra HM, Ji Y, Cohen LG& Lu B . 2010 Direct current stimulation promotes BDNF-dependent synaptic plasticity: potential implications for motor learning. Neuron 66, 198–204. (doi:10.1016/j.neuron.2010.03.035). Crossref, PubMed, Web of Science, Google Scholar - 47
Medeiros LF, de Souza IC, Vidor LP, de Souza A, Deitos A, Volz MS, Fregni F, Caumo W& Torres IL . 2012 Neurobiological effects of transcranial direct current stimulation: a review. Front. Psychiatry 3, 110. (doi:10.3389/fpsyt.2012.00110). Crossref, PubMed, Google Scholar - 48
Paulus W . 2011 Transcranial electrical stimulation (tES–tDCS; tRNS, tACS) methods. Neuropsychol. Rehabil. 21, 602–617. (doi:10.1080/09602011.2011.557292). Crossref, PubMed, Web of Science, Google Scholar - 49
Sack AT, Cohen Kadosh R, Schuhmann T, Moerel M, Walsh V& Goebel R . 2009 Optimizing functional accuracy of TMS in cognitive studies: a comparison of methods. J. Cogn. Neurosci. 21, 207–221. (doi:10.1162/jocn.2009.21126). Crossref, PubMed, Web of Science, Google Scholar - 50
Matsumoto R, Nair DR, LaPresto E, Najm I, Bingaman W, Shibasaki H& Lüders HO . 2004 Functional connectivity in the human language system: a cortico-cortical evoked potential study. Brain 127, 2316–2330. (doi:10.1093/brain/awh246). Crossref, PubMed, Web of Science, Google Scholar - 51
Kajikawa Y& Schroeder CE . 2011 How local is the local field potential? Neuron 72, 847–858. (doi:10.1016/j.neuron.2011.09.029). Crossref, PubMed, Web of Science, Google Scholar - 52
Keller CJ, Bickel S, Entz L, Ulbert I, Milham MP, Kelly C& Mehta AD . 2011 Intrinsic functional architecture predicts electrically evoked responses in the human brain. Proc. Natl Acad. Sci. USA 108, 10 308–10 313. (doi:10.1073/pnas.1019750108). Crossref, Web of Science, Google Scholar - 53
Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, Berger MS, Barbaro NM& Knight RT . 2006 High gamma power is phase-locked to theta oscillations in human neocortex. Science 313, 1626–1628. (doi:10.1126/science.1128115). Crossref, PubMed, Web of Science, Google Scholar - 54
Chang EF, Niziolek CA, Knight RT, Nagarajan SS& Houde JF . 2013 Human cortical sensorimotor network underlying feedback control of vocal pitch. Proc. Natl Acad. Sci. USA 110, 2653–2658. (doi:10.1073/pnas.1216827110). Crossref, PubMed, Web of Science, Google Scholar - 55
Crone NE, Hao L, Hart J, Boatman D, Lesser RP, Irizarry R& Gordon B . 2001 Electrocorticographic gamma activity during word production in spoken and sign language. Neurology 57, 2045–2053. (doi:10.1212/WNL.57.11.2045). Crossref, PubMed, Web of Science, Google Scholar - 56
Davidesco I, 2013 Exemplar selectivity reflects perceptual similarities in the human fusiform cortex. Cereb. Cortex 24, 1879–1893 (doi:10.1093/cercor/bht038). Crossref, PubMed, Web of Science, Google Scholar - 57
Honey CJ, 2012 Slow cortical dynamics and the accumulation of information over long timescales. Neuron 76, 423–434. (doi:10.1016/j.neuron.2012.08.011). Crossref, PubMed, Web of Science, Google Scholar - 58
Afif A, Minotti L, Kahane P& Hoffmann D . 2010 Middle short gyrus of the insula implicated in speech production: intracerebral electric stimulation of patients with epilepsy. Epilepsia 51, 206–213. (doi:10.1111/j.1528-1167.2009.02271.x). Crossref, PubMed, Web of Science, Google Scholar - 59
David O, Blauwblomme T, Job AS, Chabardes S, Hoffmann D, Minotti L& Kahane P . 2011 Imaging the seizure onset zone with stereo-electroencephalography. Brain 134, 2898–2911. (doi:10.1093/brain/awr238). Crossref, PubMed, Web of Science, Google Scholar - 60
Koubeissi MZ, Lesser RP, Sinai A, Gaillard WD, Franaszczuk PJ& Crone NE . 2012 Connectivity between perisylvian and bilateral basal temporal cortices. Cereb. Cortex 22, 918–925. (doi:10.1093/cercor/bhr163). Crossref, PubMed, Web of Science, Google Scholar - 61
Conner CR, Ellmore TM, DiSano MA, Pieters TA, Potter AW& Tandon N . 2011 Anatomic and electro-physiologic connectivity of the language system: a combined DTI-CCEP study. Comput. Biol. Med. 41, 1100–1109. (doi:10.1016/j.compbiomed.2011.07.008). Crossref, PubMed, Web of Science, Google Scholar - 62
Creutzfeldt OD, Watanabe S& Lux HD . 1966 Relations between EEG phenomena and potentials of single cortical cells. I. Evoked responses after thalamic and erpicortical stimulation. Electroencephalogr. Clin. Neurophysiol. 20, 1–18. (doi:10.1016/0013-4694(66)90136-2). Crossref, PubMed, Google Scholar - 63
Matsumoto R, Nair DR, LaPresto E, Bingaman W, Shibasaki H& Luders HO . 2007 Functional connectivity in human cortical motor system: a cortico-cortical evoked potential study. Brain 130, 181–197. (doi:10.1093/brain/awl257). Crossref, PubMed, Web of Science, Google Scholar - 64
Geschwind N . 1970 The organization of language and the brain. Science 170, 940–944. (doi:10.1126/science.170.3961.940). Crossref, PubMed, Web of Science, Google Scholar - 65
Lacruz ME, Garcia Seoane JJ, Valentin A, Selway R& Alarcon G . 2007 Frontal and temporal functional connections of the living human brain. Eur. J. Neurosci. 26, 1357–1370. (doi:10.1111/j.1460-9568.2007.05730.x). Crossref, PubMed, Web of Science, Google Scholar - 66
Matsumoto R, 2012 Parieto-frontal network in humans studied by cortico-cortical evoked potential. Hum. Brain Mapp. 33, 2856–2872. (doi:10.1002/hbm.21407). Crossref, PubMed, Web of Science, Google Scholar - 67
Kubota Y, Enatsu R, Gonzalez-Martinez J, Bulacio J, Mosher J, Burgess RC& Nair DR . 2013 In vivo human hippocampal cingulate connectivity: a corticocortical evoked potentials (CCEPs) study. Clin. Neurophysiol. 124, 1547–1556. (doi:10.1016/j.clinph.2013.01.024). Crossref, PubMed, Web of Science, Google Scholar - 68
Borchers S, Himmelbach M, Logothetis N& Karnath HO . 2012 Direct electrical stimulation of human cortex—the gold standard for mapping brain functions? Nat. Rev. Neurosci. 13, 63–70. (doi:10.1038/nrn3140). Crossref, Web of Science, Google Scholar - 69
Nathan SS, Sinha SR, Gordon B, Lesser RP& Thakor NV . 1993 Determination of current density distributions generated by electrical stimulation of the human cerebral cortex. Electroencephalogr. Clin. Neurophysiol. 86, 183–192. (doi:10.1016/0013-4694(93)90006-H). Crossref, PubMed, Google Scholar - 70
Brill J& Huguenard JR . 2009 Robust short-latency perisomatic inhibition onto neocortical pyramidal cells detected by laser-scanning photostimulation. J. Neurosci. 29, 7413–7423. (doi:10.1523/JNEUROSCI.6098-08.2009). Crossref, PubMed, Web of Science, Google Scholar - 71
Kaiser KM, Zilberter Y& Sakmann B . 2001 Back-propagating action potentials mediate calcium signalling in dendrites of bitufted interneurons in layer 2/3 of rat somatosensory cortex. J. Physiol. 535, 17–31. (doi:10.1111/j.1469-7793.2001.t01-1-00017.x). Crossref, PubMed, Web of Science, Google Scholar - 72
Stuart G, Schiller J& Sakmann B . 1997 Action potential initiation and propagation in rat neocortical pyramidal neurons. J. Physiol. 505, 617–632. (doi:10.1111/j.1469-7793.1997.617ba.x). Crossref, PubMed, Web of Science, Google Scholar - 73
Entz L, Fabo D, Eross L, Halasz P, Wittner L, Karmas G, Halgren E& Ulbert I . 2007 Inhibitory effects of cortical electrical stimulation in epilepsy patients. Neuroscience 2007, San Diego, CA, USA, 3–7 November 2007, 259.13/Q20. Washington, DC: Society for Neuroscience. Google Scholar - 74
Ezure K& Oshima T . 1985 Lateral spread of neuronal activity within the motor cortex investigated with intracellular responses to distant epicortical stimulation. Jpn. J. Physiol. 35, 223–249. (doi:10.2170/jjphysiol.35.223). Crossref, PubMed, Google Scholar - 75
Steriade M& Amzica F . 1996 Intracortical and corticothalamic coherency of fast spontaneous oscillations. Proc. Natl Acad. Sci. USA 93, 2533–2538. (doi:10.1073/pnas.93.6.2533). Crossref, PubMed, Web of Science, Google Scholar - 76
Llinás RR& Nicholson C . 1974 Analysis of field potential in the central nervous system. Handb. Electroencephalogr. Clin. Neurophysiol. 2B, 61–83. Google Scholar - 77
Mitzdorf U& Singer W . 1978 Prominent excitatory pathways in the cat visual cortex (A 17 and A 18): a current source density analysis of electrically evoked potentials. Exp. Brain Res. 33, 371–394. (doi:10.1007/BF00235560). Crossref, PubMed, Web of Science, Google Scholar - 78
Schroeder CE, Mehta AD& Givre SJ . 1998 A spatiotemporal profile of visual system activation revealed by current source density analysis in the awake macaque. Cereb. Cortex 8, 575–592. (doi:10.1093/cercor/8.7.575). Crossref, PubMed, Web of Science, Google Scholar - 79
Douglas RJ& Martin KA . 2007 Recurrent neuronal circuits in the neocortex. Curr. Biol 17, R496–R500. (doi:10.1016/j.cub.2007.04.024). Crossref, PubMed, Web of Science, Google Scholar - 80
Mehta AD, Ulbert I& Schroeder CE . 2000 Intermodal selective attention in monkeys. II: physiological mechanisms of modulation. Cereb. Cortex 10, 359–370. (doi:10.1093/cercor/10.4.359). Crossref, PubMed, Web of Science, Google Scholar - 81
Logothetis NK, Augath M, Murayama Y, Rauch A, Sultan F, Goense J, Oeltermann A& Merkle H . 2010 The effects of electrical microstimulation on cortical signal propagation. Nat. Neurosci. 13, 1283–1291. (doi:10.1038/nn.2631). Crossref, PubMed, Web of Science, Google Scholar - 82
Pollen DA . 1977 Responses of single neurons to electrical stimulation of the surface of the visual cortex. Brain Behav. Evol. 14, 67–86. (doi:10.1159/000125576). Crossref, PubMed, Web of Science, Google Scholar - 83
Godschalk M, Lemon RN, Kuypers HG& van der Steen J . 1985 The involvement of monkey premotor cortex neurones in preparation of visually cued arm movements. Behav. Brain Res. 18, 143–157. (doi:10.1016/0166-4328(85)90070-1). Crossref, PubMed, Web of Science, Google Scholar - 84
Calvin WH& Sypert GW . 1976 Fast and slow pyramidal tract neurons: an intracellular analysis of their contrasting repetitive firing properties in the cat. J. Neurophysiol. 39, 420–434. Crossref, PubMed, Web of Science, Google Scholar - 85
Finlay BL, Schiller PH& Volman SF . 1976 Quantitative studies of single-cell properties in monkey striate cortex. IV. Corticotectal cells. J. Neurophysiol. 39, 1352–1361. Crossref, PubMed, Web of Science, Google Scholar - 86
Alarcon G, Martinez J, Kerai SV, Lacruz ME, Quiroga RQ, Selway RP, Richardson MP, Garcia Seoane JJ& Valentin A . 2012 In vivo neuronal firing patterns during human epileptiform discharges replicated by electrical stimulation. Clin. Neurophysiol. 123, 1736–1744. (doi:10.1016/j.clinph.2012.02.062). Crossref, PubMed, Web of Science, Google Scholar - 87
Hill S& Tononi G . 2005 Modeling sleep and wakefulness in the thalamocortical system. J. Neurophysiol. 93, 1671–1698. (doi:10.1152/jn.00915.2004). Crossref, PubMed, Web of Science, Google Scholar - 88
Csercsa R, 2010 Laminar analysis of slow wave activity in humans. Brain 133, 2814–2829. (doi:10.1093/brain/awq169). Crossref, PubMed, Web of Science, Google Scholar - 89
Cash SS, 2009 The human K-complex represents an isolated cortical down-state. Science 324, 1084–1087. (doi:10.1126/science.1169626). Crossref, PubMed, Web of Science, Google Scholar - 90
Matsui T, Tamura K, Koyano KW, Takeuchi D, Adachi Y, Osada T& Miyashita Y . 2011 Direct comparison of spontaneous functional connectivity and effective connectivity measured by intracortical microstimulation: an fMRI study in macaque monkeys. Cereb. Cortex 21, 2348–2356. (doi:10.1093/cercor/bhr019). Crossref, PubMed, Web of Science, Google Scholar - 91
Johnston JM, Vaishnavi SN, Smyth MD, Zhang D, He BJ, Zempel JM, Shimony JS, Snyder AZ& Raichle ME . 2008 Loss of resting interhemispheric functional connectivity after complete section of the corpus callosum. J. Neurosci. 28, 6453–6458. (doi:10.1523/JNEUROSCI.0573-08.2008). Crossref, PubMed, Web of Science, Google Scholar - 92
O'Reilly JX, 2013 Causal effect of disconnection lesions on interhemispheric functional connectivity in rhesus monkeys. Proc. Natl Acad. Sci. USA 110, 13 982–13 987. (doi:10.1073/pnas.1305062110). Crossref, Web of Science, Google Scholar - 93
Greicius MD, Krasnow B, Reiss AL& Menon V . 2003 Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl Acad. Sci. USA 100, 253–258. (doi:10.1073/pnas.0135058100). Crossref, PubMed, Web of Science, Google Scholar - 94
Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA& Shulman GL . 2001 A default mode of brain function. Proc. Natl Acad. Sci. USA 98, 676–682. (doi:10.1073/pnas.98.2.676). Crossref, PubMed, Web of Science, Google Scholar - 95
Keller CJ, Honey CJ, Entz L, Bickel S, Groppe DM, Toth E, Ulbert I, Lado FA& Mehta AD . 2014 Corticocortical evoked potentials reveal projectors and integrators in human brain networks. J. Neurosci. 34, 9152–9163. (doi:10.1523/JNEUROSCI.4289-13.2014). Crossref, PubMed, Web of Science, Google Scholar - 96
Entz L, Toth E, Keller CJ, Bickel S, Groppe DM, Fabo D, Kozak LR, Eross L, Ulbert I& Mehta AD . In press. Evoked effective connectivity of the human neocortex. doi:10.1002/hbm.22581). Google Scholar - 97
Oya H, Poon PW, Brugge JF, Reale RA, Kawasaki H, Volkov IO& Howard MA . 2007 Functional connections between auditory cortical fields in humans revealed by Granger causality analysis of intra-cranial evoked potentials to sounds: comparison of two methods. Bio. Syst. 89, 198–207. (doi:10.1016/j.biosystems.2006.05.018). Google Scholar - 98
Yan C& He Y . 2011 Driving and driven architectures of directed small-world human brain functional networks. PLoS ONE 6, e23460. (doi:10.1371/journal.pone.0023460). Crossref, PubMed, Web of Science, Google Scholar - 99
Salvador R, Suckling J, Coleman MR, Pickard JD, Menon D& Bullmore E . 2005 Neurophysiological architecture of functional magnetic resonance images of human brain. Cereb. Cortex 15, 1332–1342. (doi:10.1093/cercor/bhi016). Crossref, PubMed, Web of Science, Google Scholar - 100
Sporns O& Honey CJ . 2006 Small worlds inside big brains. Proc. Natl Acad. Sci. USA 103, 19 219–19 220. (doi:10.1073/pnas.0609523103). Crossref, Web of Science, Google Scholar - 101
Kaiser M& Hilgetag CC . 2006 Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput. Biol. 2, e95. (doi:10.1371/journal.pcbi.0020095). Crossref, PubMed, Web of Science, Google Scholar - 102
Shen K, Bezgin G, Hutchison RM, Gati JS, Menon RS, Everling S& McIntosh AR . 2012 Information processing architecture of functionally defined clusters in the macaque cortex. J. Neurosci. 32, 17 465–17 476. (doi:10.1523/JNEUROSCI.2709-12.2012). Crossref, Web of Science, Google Scholar - 103
Sporns O, Honey CJ& Kotter R . 2007 Identification and classification of hubs in brain networks. PLoS ONE 2, e1049. (doi:10.1371/journal.pone.0001049). Crossref, PubMed, Web of Science, Google Scholar - 104
Manning JR, Jacobs J, Fried I& Kahana MJ . 2009 Broadband shifts in local field potential power spectra are correlated with single-neuron spiking in humans. J. Neurosci. 29, 13 613–13 620. (doi:10.1523/JNEUROSCI.2041-09.2009). Crossref, Web of Science, Google Scholar - 105
Ray S, Crone NE, Niebur E, Franaszczuk PJ& Hsiao SS . 2008 Neural correlates of high-gamma oscillations (60–200 Hz) in macaque local field potentials and their potential implications in electrocorticography. J. Neurosci. 28, 11 526–11 536. (doi:10.1523/JNEUROSCI.2848-08.2008). Crossref, Web of Science, Google Scholar - 106
Ray S& Maunsell JH . 2011 Different origins of gamma rhythm and high-gamma activity in macaque visual cortex. PLoS Biol. 9, e1000610. (doi:10.1371/journal.pbio.1000610). Crossref, PubMed, Web of Science, Google Scholar - 107
Al-ani T, Cazettes F, Palfi S& Lefaucheur JP . 2011 Automatic removal of high-amplitude stimulus artefact from neuronal signal recorded in the subthalamic nucleus. J. Neurosci. Methods 198, 135–146. (doi:10.1016/j.jneumeth.2011.03.022). Crossref, PubMed, Web of Science, Google Scholar - 108
Gilley PM, Sharma A, Dorman M, Finley CC, Panch AS& Martin K . 2006 Minimization of cochlear implant stimulus artifact in cortical auditory evoked potentials. Clin. Neurophysiol. 117, 1772–1782. (doi:10.1016/j.clinph.2006.04.018). Crossref, PubMed, Web of Science, Google Scholar - 109
Ojemann GA . 1991 Cortical organization of language. J. Neurosci. 11, 2281–2287. Crossref, PubMed, Web of Science, Google Scholar - 110
Kanwisher N, McDermott J& Chun MM . 1997 The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 17, 4302–4311. Crossref, PubMed, Web of Science, Google Scholar - 111
Epstein R& Kanwisher N . 1998 A cortical representation of the local visual environment. Nature 392, 598–601. (doi:10.1038/33402). Crossref, PubMed, Web of Science, Google Scholar - 112
Spencer SS . 2002 Neural networks in human epilepsy: evidence of and implications for treatment. Epilepsia 43, 219–227. (doi:10.1046/j.1528-1157.2002.26901.x). Crossref, PubMed, Web of Science, Google Scholar - 113
Dichter MA& Ayala GF . 1987 Cellular mechanisms of epilepsy: a status report. Science 237, 157–164. (doi:10.1126/science.3037700). Crossref, PubMed, Web of Science, Google Scholar - 114
Valentin A, Alarcón G, Honavar M, Garcia Seoane JJ, Selway RP, Polkey CE& Binnie CD . 2005 Single pulse electrical stimulation for identification of structural abnormalities and prediction of seizure outcome after epilepsy surgery: a prospective study. Lancet 4, 718–726. (doi:10.1016/S1474-4422(05)70200-3). Crossref, PubMed, Web of Science, Google Scholar - 115
Enatsu R, Piao Z, O'Connor T, Horning K, Mosher J, Burgess R, Bingaman W& Nair D . 2011 Cortical excitability varies upon ictal onset patterns in neocortical epilepsy: a cortico-cortical evoked potential study. Clin. Neurophysiol. 123, 252–260. (doi:10.1016/j.clinph.2011.06.030). Crossref, PubMed, Web of Science, Google Scholar - 116
Kahane P, Tassi L, Francione S, Hoffmann D, Lo Russo G& Munari C . 1993 Electroclinical manifestations elicited by intracerebral electric stimulation ‘shocks’ in temporal lobe epilepsy. Neurophysiol. Clin. 23, 305–326. (doi:10.1016/S0987-7053(05)80123-6). Crossref, PubMed, Google Scholar - 117
Milham MP . 2012 Open neuroscience solutions for the connectome-wide association era. Neuron 73, 214–218. (doi:10.1016/j.neuron.2011.11.004). Crossref, PubMed, Web of Science, Google Scholar - 118
David O, Job AS, De Palma L, Hoffmann D, Minotti L& Kahane P . 2013 Probabilistic functional tractography of the human cortex. Neuroimage 80, 307–317. (doi:10.1016/j.neuroimage.2013.05.075). Crossref, PubMed, Web of Science, Google Scholar