Assessing Granger Causality in Electrophysiological Data: Removing the Adverse Effects of Common Signals via Bipolar Derivations
Open accessAbstract
Multielectrode voltage data are usually recorded against a common reference. Such data are frequently used without further treatment to assess patterns of functional connectivity between neuronal populations and between brain areas. It is important to note from the outset that such an approach is valid only when the reference electrode is nearly electrically silent. In practice, however, the reference electrode is generally not electrically silent, thereby adding a common signal to the recorded data. Volume conduction further complicates the problem. In this study we demonstrate the adverse effects of common signals on the estimation of Granger causality, which is a statistical measure used to infer synaptic transmission and information flow in neural circuits from multielectrode data. We further test the hypothesis that the problem can be overcome by utilizing bipolar derivations where the difference between two nearby electrodes is taken and treated as a representation of local neural activity. Simulated data generated by a neuronal network model where the connectivity pattern is known were considered first. This was followed by analyzing data from three experimental preparations where a priori predictions regarding the patterns of causal interactions can be made: (1) laminar recordings from the hippocampus of an anesthetized rat during theta rhythm, (2) laminar recordings from V4 of an awake-behaving macaque monkey during alpha rhythm, and (3) ECoG recordings from electrode arrays implanted in the middle temporal lobe and prefrontal cortex of an epilepsy patient during fixation. For both simulation and experimental analysis the results show that bipolar derivations yield the expected connectivity patterns whereas the untreated data (referred to as unipolar signals) do not. In addition, current source density signals, where applicable, yield results that are close to the expected connectivity patterns, whereas the commonly practiced average re-reference method leads to erroneous results.
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Bipolar derivation was used prior to Granger causality and coherence analysis to avoid spurious results from a common reference.
“Bipolar derivation is a recommended prestep prior to Granger causality and coherence analysis, as the presence of a common reference can lead to spurious results (73, 74).”
From Layer and rhythm specificity for predictive routing (2020) · cites this paper as [73]
The Conclusion (page unavailable) says a common reference can confound Granger causality and proposes bipolar derivations to overcome the problem. Discussion > Additional remarks (page unavailable) explicitly recommends bipolar derivation as a post hoc step before computing connectivity measures such as Granger causality. The paper does not specifically establish the recommendation for coherence analysis. (LLM, conf=0.85)
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Cites
A new look at the statistical model identification
Akaike, H. (1974) · IEEE Transactions on Automatic Control · doi:10.1109/tac.1974.1100705 · Cited by 51,879 · see citing works
Investigating causal relations by econometric models and cross-spectral methods
Granger, C. W. J. (1969) · Econometrica · doi:10.2307/1912791 · Cited by 22,989 · see citing works
Investigating Causal Relations by Econometric Models and Cross-Spectral Methods
Granger, C. W. J. (2010) · Essays in Econometrics · doi:10.1017/cbo9780511753978.002 · Cited by 4,762 · see citing works
The three-dimensional organization of the hippocampal formation: A review of anatomical data
Amaral, D. G., & Witter, M. P. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90424-7 · Cited by 2,180 · see citing works
NEURONAL CIRCUITS OF THE NEOCORTEX
Douglas, R. J., & Martin, K. A. C. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144152 · Cited by 1,886 · see citing works
Identifying true brain interaction from EEG data using the imaginary part of coherency
Nolte, G., Bai, O., Wheaton, L., Mari, Z., Vorbach, S., & Hallett, M. (2004) · Clinical Neurophysiology · doi:10.1016/j.clinph.2004.04.029 · Cited by 1,756 · see citing works
Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection
Lakatos, P., Karmos, G., Mehta, A. D., Ulbert, I., & Schroeder, C. E. (2008) · Science · doi:10.1126/science.1154735 · Cited by 1,719 · see citing works
Self-citationMitzdorf, U. (1985) · Physiological Reviews · doi:10.1152/physrev.1985.65.1.37 · Cited by 1,690 · see citing works
Nunez, P. L., Srinivasan, R., Westdorp, A. F., Wijesinghe, R. S., Tucker, D. M., Silberstein, R. B., & Cadusch, P. J. (1997) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/s0013-4694(97)00066-7 · Cited by 1,230 · see citing works
Neural mechanisms underlying brain waves: from neural membranes to networks
Lopes da Silva, F. (1991) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(91)90044-5 · Cited by 1,112 · see citing works
Kamiński, M., Ding, M., Truccolo, W., & Bressler, S. L. (2001) · Biological Cybernetics · doi:10.1007/s004220000235 · Cited by 990 · see citing works
Self-citationMechanisms of Gamma Oscillations in the Hippocampus of the Behaving Rat
Csicsvari, J., Jamieson, B. G., Wise, K. D., & Buzsáki, G. (2003) · Neuron · doi:10.1016/s0896-6273(02)01169-8 · Cited by 990 · see citing works
The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies)
Amaral, D. G., Scharfman, H. E., & Lavenex, P. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)63001-5 · Cited by 888 · see citing works
Nicholson, C., & Freeman, J. A. (1975) · Journal of Neurophysiology · doi:10.1152/jn.1975.38.2.356 · Cited by 699 · see citing works
Intrinsic Oscillations of Neocortex Generated by Layer 5 Pyramidal Neurons
Silva, L. R., Amitai, Y., & Connors, B. W. (1991) · Science · doi:10.1126/science.1824881 · Cited by 682 · see citing works
Granger Causality: Basic Theory and Application to Neuroscience
Ding, M., Chen, Y., & Bressler, S. L. (2006) · doi:10.1002/9783527609970.ch17 · Cited by 669 · see citing works
Self-citationHow Local Is the Local Field Potential?
Kajikawa, Y., & Schroeder, C. E. (2011) · Neuron · doi:10.1016/j.neuron.2011.09.029 · Cited by 584 · see citing works
Self-citationDing, M., Bressler, S. L., Yang, W., & Liang, H. (2000) · Biological Cybernetics · doi:10.1007/s004229900137 · Cited by 582 · see citing works
Self-citationLocal Origin of Field Potentials in Visual Cortex
Katzner, S., Nauhaus, I., Benucci, A., Bonin, V., Ringach, D. L., & Carandini, M. (2009) · Neuron · doi:10.1016/j.neuron.2008.11.016 · Cited by 552 · see citing works
Evidence from Functional Neuroimaging of a Compensatory Prefrontal Network in Alzheimer's Disease
Grady, C. L., McIntosh, A. R., Beig, S., Keightley, M., Burian, H., & Black, S. E. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-03-00986.2003 · Cited by 504 · see citing works
TUTORIAL ON NEUROBIOLOGY: FROM SINGLE NEURONS TO BRAIN CHAOS
Freeman, W. J. (1992) · International Journal of Bifurcation and Chaos · doi:10.1142/s0218127492000653 · Cited by 496 · see citing works
Schroeder, C. (1998) · Cerebral Cortex · doi:10.1093/cercor/8.7.575 · Cited by 464 · see citing works
Self-citationNeuronal Mechanisms and Attentional Modulation of Corticothalamic Alpha Oscillations
Bollimunta, A., Mo, J., Schroeder, C. E., & Ding, M. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.5580-10.2011 · Cited by 441 · see citing works
Self-citationNeuronal Mechanisms of Cortical Alpha Oscillations in Awake-Behaving Macaques
Bollimunta, A., Chen, Y., Schroeder, C. E., & Ding, M. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.2699-08.2008 · Cited by 434 · see citing works
Self-citationUsing a Common Average Reference to Improve Cortical Neuron Recordings From Microelectrode Arrays
Ludwig, K. A., Miriani, R. M., Langhals, N. B., Joseph, M. D., Anderson, D. J., & Kipke, D. R. (2008) · Journal of Neurophysiology · doi:10.1152/jn.90989.2008 · Cited by 410 · see citing works
Vertes, R. P., Hoover, W. B., Szigeti‐Buck, K., & Léránth, C. (2007) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2006.12.002 · Cited by 345 · see citing works
Functional connectivity during working memory maintenance
GAZZALEY, A., RISSMAN, J., & D'ESPOSITO, M. (2004) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/cabn.4.4.580 · Cited by 337 · see citing works
EEG coherency II: experimental comparisons of multiple measures
Nunez, P. L., Silberstein, R. B., Shi, Z., Carpenter, M. R., Srinivasan, R., Tucker, D. M., Doran, S. M., Cadusch, P. J., & Wijesinghe, R. S. (1999) · Clinical Neurophysiology · doi:10.1016/s1388-2457(98)00043-1 · Cited by 316 · see citing works
Tenke, C. E., & Jürgen Kayser, A. (2012) · Clinical Neurophysiology · doi:10.1016/j.clinph.2012.06.005 · Cited by 270 · see citing works
Intermodal Selective Attention in Monkeys. I: Distribution and Timing of Effects across Visual Areas
Mehta, A. D. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.4.343 · Cited by 267 · see citing works
Anderson, K. L., Rajagovindan, R., Ghacibeh, G. A., Meador, K. J., & Ding, M. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp223 · Cited by 222 · see citing works
Self-citationInterdependence of Multiple Theta Generators in the Hippocampus: a Partial Coherence Analysis
Kocsis, B., Bragin, A., & Buzsáki, G. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-14-06200.1999 · Cited by 218 · see citing works
Self-citationMima, T., & Hallett, M. (1999) · Clinical Neurophysiology · doi:10.1016/s1388-2457(99)00238-2 · Cited by 210 · see citing works
Haegens, S., Barczak, A., Musacchia, G., Lipton, M. L., Mehta, A. D., Lakatos, P., & Schroeder, C. E. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0600-15.2015 · Cited by 204 · see citing works
Self-citationRempel-Clower, N. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.9.851 · Cited by 203 · see citing works
Cassel, J., de Vasconcelos, A. P., Loureiro, M., Cholvin, T., Dalrymple‐Alford, J. C., & Vertes, R. P. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.08.006 · Cited by 202 · see citing works
Brovelli, A., Lachaux, J.-P., Kahane, P., & Boussaoud, D. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.05.045 · Cited by 160 · see citing works
Neural correlates of access to short-term memory
Nee, D. E., & Jonides, J. J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802081105 · Cited by 158 · see citing works
Functional anatomy and interaction of fast and slow visual pathways in macaque monkeys
Chen, C.-M., Lakatos, P., Shah, A. S., Mehta, A. D., Givre, S. J., Javitt, D. C., & Schroeder, C. E. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhl067 · Cited by 155 · see citing works
Self-citationCorrelated Variability in Laminar Cortical Circuits
Hansen, B. J., Chelaru, M. I., & Dragoi, V. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.029 · Cited by 146 · see citing works
Flint, A. C., & Connors, B. W. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.75.2.951 · Cited by 143 · see citing works
Newman, E. L., Gillet, S. N., Climer, J. R., & Hasselmo, M. E. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2586-13.2013 · Cited by 137 · see citing works
Contribution of extrastriate area V4 to the surface-recorded flash VEP in the awake macaque
Givre, S. J., Schroeder, C. E., & Arezzo, J. C. (1994) · Vision Research · doi:10.1016/0042-6989(94)90156-2 · Cited by 133 · see citing works
Self-citationOngoing physiological processes in the cerebral cortex
Leopold, D. A., & Maier, A. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.10.059 · Cited by 127 · see citing works
A Neocortical Delta Rhythm Facilitates Reciprocal Interlaminar Interactions via Nested Theta Rhythms
Carracedo, L. M., Kjeldsen, H., Cunnington, L. G., Jenkins, A., Schofield, I. S., Cunningham, M. O., Davies, C. H., Traub, R. D., & Whittington, M. A. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0735-13.2013 · Cited by 113 · see citing works
Barbas, H., Medalla, M., Alade, O., Suski, J., Zikopoulos, B., & Lera, P. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi018 · Cited by 112 · see citing works
Audoin, B., Guye, M., Françoise Reuter, A., Duong, M.-V. A., Sylviane Confort-gouny, A., Irina Malikova, A., Soulier, E., Viout, P., Cherif, A. A., Cozzone, P. J., et al. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.04.038 · Cited by 111 · see citing works
Localization of ERP generators and identification of underlying neural processes.
Schroeder, C. E., Steinschneider, M., Dc, J., Tenke, C. E., Givre, S. J., Mehta, A. D., Simpson, G. V., Arezzo, J. C., & Hg, V. (1995) · PubMed · Cited by 106 · see citing works
Self-citationSteinmetz, N. A., & Moore, T. (2014) · Neuron · doi:10.1016/j.neuron.2014.06.014 · Cited by 104 · see citing works
Septo-hippocampal pathway necessary for dentate theta production
Andersen, P. N., Bland, H. B., Myhrer, T., et al. (1979) · Brain Research · doi:10.1016/0006-8993(79)90040-4 · Cited by 103 · see citing works
Mitigating the effects of measurement noise on Granger causality
Nalatore, H., Ding, M., & Rangarajan, G. (2007) · Physical Review E · doi:10.1103/physreve.75.031123 · Cited by 98 · see citing works
Self-citationGodlove, D. C., Maier, A., Woodman, G. F., & Schall, J. D. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.5127-13.2014 · Cited by 88 · see citing works
Effect of Stimulus Size on the Dynamics of Orientation Selectivity in Macaque V1
Xing, D., Shapley, R. M., Hawken, M. J., & Ringach, D. L. (2005) · Journal of Neurophysiology · doi:10.1152/jn.01139.2004 · Cited by 85 · see citing works
Pohlmeyer, E. A., Mahmoudi, B., Geng, S., Prins, N. W., & Sanchez, J. C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087253 · Cited by 76 · see citing works
Kajikawa, Y., & Schroeder, C. E. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00914.2013 · Cited by 47 · see citing works
Self-citationRajagovindan, R., & Ding, M. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003649 · Cited by 39 · see citing works
Self-citationKorovaichuk, A., Makarova, J., Makarov, V. A., et al. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00297.2010 · Cited by 39 · see citing works
Treves, A. (2016) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198749783.003.0005 · Cited by 30 · see citing works
On the Estimation of Population-Specific Synaptic Currents from Laminar Multielectrode Recordings
Gratiy, S. L., Devor, A., Einevoll, G. T., & Dale, A. M. (2011) · Frontiers in Neuroinformatics · doi:10.3389/fninf.2011.00032 · Cited by 28 · see citing works
Denoising neural data with state-space smoothing: Method and application
Nalatore, H., Ding, M., & Rangarajan, G. (2009) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2009.01.013 · Cited by 27 · see citing works
Self-citationShahbazi, F., Ewald, A., Ziehe, A., et al. (2010) · World Congress on Medical Physics and Biomedical Engineering, September 7 - 12, 2009, Munich, Germany · doi:10.1007/978-3-642-12197-5_46 · Cited by 24 · see citing works
Characterizing Oscillatory Cortical Networks with Granger Causality
Bollimunta, A., Chen, Y., Schroeder, C. E., & Ding, M. (2009) · Springer eBooks · doi:10.1007/978-1-4419-0389-1_9 · Cited by 16 · see citing works
Self-citationSpecificity and non-specificity of synaptic connections within mammalian visual cortex
Lund, J. S. (2002) · Journal of Neurocytology · doi:10.1023/a:1024161623560 · Cited by 15 · see citing works
Kapoor, V., Krampe, E., Klug, A., et al. (2013) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2013.03.017 · Cited by 4 · see citing works
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Research works printed but not linked: 1
- Wiener N. (1956). The theory of prediction, in Modern Mathematics for Engineers, Vol. 1, ed Beckenbach E. F. (New York, NY: McGraw-Hill), 125– 139.
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“Bipolar derivation is a recommended prestep prior to Granger causality and coherence analysis, as the presence of a common reference can lead to spurious results (73, 74).”
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- Authors
- Trongnetrpunya, A., Nandi, B., Kang, D., Kocsis, B., Schroeder, C. E., & Ding, M.
- Affiliations
- University of Florida (US)
- Nathan Kline Institute for Psychiatric Research (US)
- Corresponding author
- Ding, Mingzhou
- Venue
- Frontiers in Systems Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2016-01-20
- Volume
- 9
- Pages
- 189-189
- ISSN
- 1662-5137 (ISSN-L)
- PMC
- PMC4718991
- OpenAlex
- W2272545495
- Cited by
- 75
- References
- 64
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 5 · 2023: 4 · 2022: 9 · 2021: 9 · 2020: 8 · 2019: 11 · 2018: 17 · 2017: 6 · 2016: 1 · 2014: 1
- FWCI
- 7.42
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Systems Neuroscience (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health (MH097320, MH100820, MH103814, DC011490)
- National Science Foundation (BCS-1439188)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neural Engineering
- Keywords
- Granger causality, reference electrode, volume conduction, multi-electrode recording, functional connectivity, current source density, theta oscillations, alpha rhythm, electrocorticography, hippocampus, area V4, epilepsy, neural circuits
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