Abstract
A significant challenge in modern neuroscience lies in determining the functional connectivity between discrete populations of neurones and brain regions. In this study, a variation of partial directed coherence, the generalized partial directed coherence (gPDC), along with a newly proposed critical value for gPDC, were applied on recorded local field potentials (LFPs) and single-unit activity, in order to assess information flow between medial prefrontal cortex (mPFC) and hippocampus and within the hippocampus of the rat brain, under isoflurane anesthesia and kainic acid-induced enhanced neuronal activity. Our findings suggest that, under anesthesia, there exists a continuous information flow from hippocampus towards mPFC, reversed mostly during activity bursts occurring in the mPFC. Moreover, there was a clear directional connection from the lateral towards medial dorsal hippocampus, most prominent in the beta frequency band (10–30 Hz). Kainic acid resulted in partially disrupting the reciprocal cortico-hippocampal connectivity and reversing the intra-hippocampal one. The biological implications of these findings on the effects of anesthesia and kainic acid in brain connectivity, along with implementation issues of gPDC analysis on field potentials and spike trains, are extensively discussed.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19(6): 716–723
Amaral D, Witter M (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31(3): 571–591
Astolfi L, Cincotti F, Mattia D, Marciani M, Baccala L, de Vico Fallani F, Salinari S, Ursino M, Zavaglia M, Ding L et al (2007) Comparison of different cortical connectivity estimators for high-resolution EEG recordings. Hum Brain Mapp 28(2): 143
Baccalá L, Sameshima K (2001) Partial directed coherence: a new concept in neural structure determination. Biol Cybern 84(6): 463–474
Baccala L, Takahashi D, Sameshima K (2007) Generalized partial directed coherence. In: 15th international conference on digital signal processing, pp 163–166
Ben-Ari Y (1985) Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14(2): 375–403
Ben-Ari Y, Cossart R (2000) Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci 23(11): 580–587
Bernasconi C, König P (1999) On the directionality of cortical interactions studied by structural analysis of electrophysiological recordings. Biol Cybern 81(3):199–210
Brovelli A, Ding M, Ledberg A, Chen Y, Nakamura R, Bressler S (2004) Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. Proc Natl Acad Sci 101(26): 9849–9854
Buchanan S, Thompson R, Maxwell B, Powell D (1994) Efferent connections of the medial prefrontal cortex in the rabbit. Exp Brain Res 79(2): 469–483
Buckmaster P, Dudek F (1999) In vivo intracellular analysis of granule cell axon reorganization in epileptic rats. J Neurophysiol 81(2): 712–721
Cadotte A, DeMarse T, He P, Ding M (2008) Causal measures of structure and plasticity in simulated and living neural networks. PLoS ONE 3(10): 1–14
Carr D, Sesack S (1996) Hippocampal afferents to the rat prefrontal cortex: synaptic targets and relation to dopamine terminals. J Comp Neurol 369(1): 1–15
Clarke V, Ballyk B, Hoo K, Mandelzys A, Pellizzari A, Bath C, Thomas J, Sharpe E, Davies C, Ornstein P et al (1997) A GluR5 kainate receptor that regulates inhibitory synaptic transmission in the hippocampus. Nature 389: 599–603
Coomber B, O’Donoghue M, Mason R (2008) Inhibition of endocannabinoid metabolism attenuates enhanced hippocampal neuronal activity induced by kainic acid. Synapse 62(10): 746–755
Cossart R, Tyzio R, Dinocourt C, Esclapez M, Hirsch J, Ben-Ari Y, Bernard C (2001) Presynaptic kainate receptors that enhance the release of GABA on CA1 hippocampal interneurons. Neuron 29(2): 497–508
Ding M, Bressler S, Yang W, Liang H (2000) Short-window spectral analysis of cortical event-related potentials by adaptive multivariate autoregressive modeling: data preprocessing, model validation, and variability assessment. Biol Cybern 83(1): 35–45
Fanselow E, Sameshima K, Baccala L, Nicolelis M (2001) Thalamic bursting in rats during different awake behavioral states. Proc Natl Acad Sci 98(26): 15330–15335
Ferino F, Thierry A, Glowinski J (1987) Anatomical and electrophysiological evidence for a direct projection from Ammon’s horn to the medial prefrontal cortex in the rat. Exp Brain Res 65(2): 421–426
Frank L, Brown E, Wilson M (2001) A comparison of the firing properties of putative excitatory and inhibitory neurons from CA1 and the entorhinal cortex. J Neurophysiol 86(4): 2029–2040
French A, Holden A (1971) Alias-free sampling of neuronal spike trains. Biol Cybern 8(5): 165–171
Goldman-Rakic P (1995) Cellular basis of working memory. Neuron 14(3): 477–485
Goldman-Rakic P, Selemon L, Schwartz M (1984) Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocampal cortex in the rhesus monkey. Neuroscience 12(3): 719–743
Gourévitch B, Bouquin-Jeannès R, Faucon G (2006) Linear and nonlinear causality between signals: methods, examples and neurophysiological applications. Biol Cybern 95(4): 349–369
Granger CWJ (1980) Investigating causal relations by econometric models and cross-spectral methods. Econometrica 37: 424–438
Halliday D, Rosenberg J, Amjad A, Breeze P, Conway B, Farmer S (1995) A framework for the analysis of mixed time series/point process data—theory and application to the study of physiological tremor, single motor unit discharges and electromyograms. Prog Biophys Mol Biol 64(2–3): 237–278
Hong L, Mubarak W, Sunami Y, Murakami S, Fuyama Y, Ohtsuka A, Murakami T (2000) Enhanced visualization of weak colloidal iron signals with Bodians protein silver for demonstration of perineuronal nets of proteoglycans in the central nervous system. Arch Histol Cytol 63(5): 459–465
Huang J, Chang J, Woodward D, Baccalá L, Han J, Wang J, Luo F (2006) Dynamic neuronal responses in cortical and thalamic areas during different phases of formalin test in rats. Exp Neurol 200(1): 124–134
Hurley K, Herbert H, Moga M, Saper C (1991) Efferent projections of the infralimbic cortex of the rat. J Comp Neurol 308(2): 249–276
Isomura Y, Sirota A, Özen S, Montgomery S, Mizuseki K, Henze D, Buzsáki G (2006) Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron 52(5): 871–882
Jansen B (1991) Time series analysis by means of linear modelling. Tech Behav Neural Sci 5: 157–180
Jay T, Witter M (1991) Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. J Comp Neurol 313(4): 574–586
Jay T, Glowinski J, Thierry A (1989) Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat. Brain Res 505(2): 337–340
Jay T, Burette F, Laroche S (1995) NMDA receptor-dependent long-term potentiation in the hippocampal afferent fibre system to the prefrontal cortex in the rat. Eur J Neurosci 7(2): 247–250
Kamiński M, Blinowska K (1991) A new method of the description of the information flow in the brain structures. Biol Cybern 65(3): 203–210
Kamiński M, Ding M, Truccolo W, Bressler S (2001) Evaluating causal relations in neural systems: Granger causality, directed transfer function and statistical assessment of significance. Biol Cybern 85(2): 145–157
Kunz T, Oliw E (2001) The selective cyclooxygenase-2 inhibitor rofecoxib reduces kainate-induced cell death in the rat hippocampus. Eur J Neurosci 13(3): 569–575
Kus R, Kaminski M, Blinowska K (2004) Determination of EEG activity propagation: pair-wise versus multichannel estimate. IEEE Trans Biomed Eng 51(9): 1501–1510
Laroche S, Jay T, Thierry A (1990) Long-term potentiation in the prefrontal cortex following stimulation of the hippocampal CA1/subicular region. Neuroscience Lett 114(2): 184–190
Lothman E, Collins R, Ferrendelli J (1981) Kainic acid-induced limbic seizures: electrophysiologic studies. Neurology 31(7): 806–812
Lütkepohl H (2005) New introduction to multiple time series analysis. Springer, Berlin
Maingret F, Lauri S, Taira T, Isaac J (2005) Profound regulation of neonatal CA1 rat hippocampal GABAergic transmission by functionally distinct kainate receptor populations. J Physiol 567(1): 131–142
Marple S (1987) Digital spectral analysis. Prentice-Hall, Englewood Cliffs, NJ
Molle M, Yeshenko O, Marshall L, Sara S, Born J (2006) Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. J Neurophysiol 96(1): 62–70
Mulle C, Sailer A, Swanson G, Brana C, O’Gorman S, Bettler B, Heinemann S (2000) Subunit composition of kainate receptors in hippocampal interneurons. Neuron 28(2): 475–484
Nadler J (1981) Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci 29: 2031–2042
Neumaier A, Schneider T (2001) Estimation of parameters and eigenmodes of multivariate autoregressive models. ACM Trans Math Softw (TOMS) 27(1): 27–57
Paterka R, Sanderson A, O’leary D (1978) Practical considerations in the implementation of the French-Holden algorithm for sampling of neuronal spike trains. IEEE Trans Biomed Eng 25:192–195
Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, 4th edn. Academic Press, San Diego, CA
Pereda E, Quiroga R, Bhattacharya J (2005) Nonlinear multivariate analysis of neurophysiological signals. Prog Neurobiol 77(1–2): 1–37
Rodríguez-Moreno A, Herreras O, Lerma J (1997) Kainate receptors presynaptically downregulate GABAergic inhibition in the rat hippocampus. Neuron 19(4): 893–902
Room P, Russchen F, Groenewegen H, Lohman A (1985) Efferent connections of the prelimbic (area 32) and the infralimbic (area 25) cortices: an anterograde tracing study in the cat. J Comp Neurol 242(1): 40–55
Sameshima K, Baccalá L (1999) Using partial directed coherence to describe neuronal ensemble interactions. J Neurosci Methods 94(1): 93–103
Schelter B, Winterhalder M, Eichler M, Peifer M, Hellwig B, Guschlbauer B, Lücking C, Dahlhaus R, Timmer J (2006a) Testing for directed influences among neural signals using partial directed coherence. J Neurosci Methods 152(1–2): 210–219
Schelter B, Winterhalder M, Hellwig B, Guschlbauer B, Lücking C, Timmer J (2006b) Direct or indirect? Graphical models for neural oscillators. J Physiol Paris 99(1): 37–46
Schmitz D, Mellor J, Nicoll R (2001) Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses. Science 291(5510): 1972–1976
Schneider T, Neumaier A (2001) Algorithm 808: ARfit A Matlab package for the estimation of parameters and eigenmodes of multivariate autoregressive models. ACM Trans Math Softw (TOMS) 27(1): 58–65
Schubert M, Siegmund H, Pape H, Albrecht D (2005) Kindling-induced changes in plasticity of the rat amygdala and hippocampus. Learn Memory 12(5): 520–526
Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6(2): 461–464
Sesack S, Deutch A, Roth R, Bunney B (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 290(2): 213–242
Steriade M (2006) Grouping of brain rhythms in corticothalamic systems. Neuroscience 137(4): 1087–1106
Steriade M, Nunez A, Amzica F (1993) A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci 13(8): 3252–3265
Stevenson C, Halliday D, Marsden C, Mason R (2007) Systemic administration of the benzodiazepine receptor partial inverse agonist FG-7142 disrupts corticolimbic network interactions. Synapse 61(8): 646–663
Takagishi M, Chiba T (1991) Efferent projections of the infralimbic (area 25) region of the medial prefrontal cortex in the rat: an anterograde tracer PHA-L study. Brain Res 566(1–2): 26–39
Takahashi D, Baccalá L (2007) Connectivity inference between neural structures via partial directed coherence. J Appl Stat 34(10): 1259–1273
Tierney P, Degenetais E, Thierry A, Glowinski J, Gioanni Y (2004) Influence of the hippocampus on interneurons of the rat prefrontal cortex. Eur J Neurosci 20(2): 514–524
Tononi G, Massimini M, Riedner B (2006) Sleepy dialogues between cortex and hippocampus: who talks to whom?. Neuron 52(5): 748–749
Vertes R (2006) Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 142(1): 1–20
Vertes R, Hoover W, Szigeti-Buck K, Leranth C (2007) Nucleus reuniens of the midline thalamus: link between the medial prefrontal cortex and the hippocampus. Brain Res Bull 71(6): 601–609
Wang J, Chang J, Woodward D, Baccala L, Han J, Luo F (2007) Corticofugal influences on thalamic neurons during nociceptive transmission in awake rats. Synapse 61(5): 335–342
Wang J, Zhang H, Chang J, Woodward D, Baccalá L, Luo F (2008) Anticipation of pain enhances the nociceptive transmission and functional connectivity within pain network in rats. Mol Pain 4(1): 34
Westbrook G, Lothman E (1983) Cellular and synaptic basis of kainic acid-induced hippocampal epileptiform activity. Brain Res 273(1): 97–109
Winterhalder M, Schelter B, Hesse W, Schwab K, Leistritz L, Klan D, Bauer R, Timmer J, Witte H (2005) Comparison of linear signal processing techniques to infer directed interactions in multivariate neural systems. Signal Process 85(11): 2137–2160
Yang H, Chang J, Woodward D, Baccalá L, Han J, Luo F (2005) Coding of peripheral electrical stimulation frequency in thalamocortical pathways. Exp Neurol 196(1): 138–152
Open Access
This article is distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution,and reproduction in any medium, provided the original author(s) and source are credited.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
Open Access This is an open access article distributed under the terms of the Creative Commons Attribution Noncommercial License (https://creativecommons.org/licenses/by-nc/2.0), which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.
About this article
Cite this article
Taxidis, J., Coomber, B., Mason, R. et al. Assessing cortico-hippocampal functional connectivity under anesthesia and kainic acid using generalized partial directed coherence. Biol Cybern 102, 327–340 (2010). https://doi.org/10.1007/s00422-010-0370-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00422-010-0370-1