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Spatial coherence and stationarity of local field potentials in an isolated whole hippocampal preparation in vitro

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Abstract

Local field potential (LFP) multielectrode recordings of spontaneous rhythms in an isolated whole hippocampal preparation are characterized with respect to their spatial variability within the hippocampus, and their frequency properties. Using simulated data, we categorize potential relationships between frequency variation over time in LFP recordings and spatial variability between electrodes. We then use data recorded from the intact preparation to distinguish between our theoretical categories. We find that the LFP recordings have a close to spatially invariant frequency distribution (not phase) across the hippocampus, and differ in frequency only in a component that may be seen as physiological noise. From these facts, we conclude that the isolated hippocampal LFP recordings represent a single signal and may be regarded as a unitary circuitry. We additionally examine phase differences across our recording sites. We use our characterization of the hippocampal isolate’s properties to predict its spatial coherence in response to high frequency stimulation. We find that there is a finely tuned inverse relationship between temporal variability in the hippocampal isolate’s LFP recordings and their spatial coherence.

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References

  • Akay, M. (Ed.). (1998). Time frequency and wavelets in biomedical signal processing. New York: IEEE Press.

    Google Scholar 

  • Amaral, D. G., & Witter, M. P. (1989). The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience, 31, 571–591.

    Article  CAS  PubMed  Google Scholar 

  • Andersen, P., Morris, R., Amaral, D., Bliss, T., & O'Keefe, J. (2007). The hippocampus book. New York: Oxford University Press.

    Google Scholar 

  • Andersen, P., Soleng, A. F., & Raastad, M. (2000). The hippocampal lamella hypothesis revisited. Brain Research, 886, 165–171.

    Article  CAS  PubMed  Google Scholar 

  • Azarmgin S (2007) An investigation of the size of tissue required for generation of spontaneous network rhythms in an intact hippocampal preparation. In: Electrical and Computer Engineering, vol. Masters of Science, p 61 Toronto: University of Toronto.

  • Berens, P., Keliris, G. A., Ecker, A. S., Logothetis, N. K., & Tolias, A. S. (2008). Comparing the feature selectivity of the gamma-band of the local field potential and the underlying spiking activity in primate visual cortex. Front Syst Neurosci, 2, 2.

    Article  PubMed  Google Scholar 

  • Buzsaki, G. (2006). Rhythms of the brain. New York: Oxford University Press.

    Book  Google Scholar 

  • Buzsaki, G., & Chrobak, J. J. (2005). (Synaptic plasticity and self-organization in the hippocampus. Nature Neuroscience, 8, 1418–1420.

    Article  CAS  PubMed  Google Scholar 

  • Choi, H. (1989). Williams WJ (Improved time-frequency representation of multicomponent signals using exponential kernels. IEEE Trans Acoustics, Speech, Signal Processing, 37, 10.

    Article  Google Scholar 

  • Colgin, L. L., Kubota, D., Brucher, F. A., Jia, Y., Branyan, E., Gall, C. M., et al. (2004). (Spontaneous waves in the dentate gyrus of slices from the ventral hippocampus. Journal of Neurophysiol, 92, 3385–3398.

    Article  CAS  Google Scholar 

  • Gillis, J. A., Luk, W. P., Zhang, L., & Skinner, F. K. (2005). (Decomposing rhythmic hippocampal data to obtain neuronal correlates. Journal of Neuroscience Methods, 147, 99–113.

    Article  CAS  PubMed  Google Scholar 

  • Hampson, R. E., Simeral, J. D., & Deadwyler, S. A. (1999). (Distribution of spatial and nonspatial information in dorsal hippocampus. Nature, 402, 610–614.

    Article  CAS  PubMed  Google Scholar 

  • Henrie, J. A., & Shapley, R. (2005). (LFP power spectra in V1 cortex: the graded effect of stimulus contrast. Journal of Neurophysiol, 94, 479–490.

    Article  Google Scholar 

  • Holscher, C., Anwyl, R., & Rowan, M. J. (1997). (Stimulation on the positive phase of hippocampal theta rhythm induces long-term potentiation that can Be depotentiated by stimulation on the negative phase in area CA1 in vivo. Journal of Neuroscience, 17, 6470–6477.

    CAS  PubMed  Google Scholar 

  • Jarosiewicz, B., McNaughton, B. L., & Skaggs, W. E. (2002). (Hippocampal population activity during the small-amplitude irregular activity state in the rat. Journal of Neuroscience, 22, 1373–1384.

    CAS  PubMed  Google Scholar 

  • Jones, M. W., & Wilson, M. A. (2005). (Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol, 3, e402.

    Article  PubMed  Google Scholar 

  • Katzner, S., Nauhaus, I., Benucci, A., Bonin, V., Ringach, D. L., & Carandini, M. (2009). (Local origin of field potentials in visual cortex. Neuron, 61, 35–41.

    Article  CAS  PubMed  Google Scholar 

  • Khalilov, I., Esclapez, M., Medina, I., Aggoun, D., Lamsa, K., Leinekugel, X., et al. (1997). (A novel in vitro preparation: the intact hippocampal formation. Neuron, 19, 743–749.

    Article  CAS  PubMed  Google Scholar 

  • Kowalczyk, T., Golebiewski, H., & Konopacki, J. (2009). (Is the dentate gyrus an independent generator of in vitro recorded theta rhythm? Brain Research Bulletin, 80, 139–146.

    Article  PubMed  Google Scholar 

  • Kramis, R., Vanderwolf, C. H., & Bland, B. H. (1975). (Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital. Experimental Neurology, 49, 58–85.

    Article  CAS  PubMed  Google Scholar 

  • Kreiman, G., Hung, C. P., Kraskov, A., Quiroga, R. Q., Poggio, T., & DiCarlo, J. J. (2006). (Object selectivity of local field potentials and spikes in the macaque inferior temporal cortex. Neuron, 49, 433–445.

    Article  CAS  PubMed  Google Scholar 

  • Linkenkaer-Hansen, K., Nikouline, V. V., Palva, J. M., & Ilmoniemi, R. J. (2001). (Long-range temporal correlations and scaling behavior in human brain oscillations. Journal of Neuroscience, 21, 1370–1377.

    CAS  PubMed  Google Scholar 

  • Liu, J., & Newsome, W. T. (2006). (Local field potential in cortical area MT: stimulus tuning and behavioral correlations. Journal of Neuroscience, 26, 7779–7790.

    Article  CAS  PubMed  Google Scholar 

  • Logothetis, N. K. (2003). (The underpinnings of the BOLD functional magnetic resonance imaging signal. Journal of Neuroscience, 23, 3963–3971.

    CAS  PubMed  Google Scholar 

  • Logothetis, N. K., Kayser, C., & Oeltermann, A. (2007). (In vivo measurement of cortical impedance spectrum in monkeys: implications for signal propagation. Neuron, 55, 809–823.

    Article  CAS  PubMed  Google Scholar 

  • Logothetis, N. K., Pauls, J., Augath, M., Trinath, T., & Oeltermann, A. (2001). (Neurophysiological investigation of the basis of the fMRI signal. Nature, 412, 150–157.

    Article  CAS  PubMed  Google Scholar 

  • Lubenov, E. V., & Siapas, A. G. (2009). (Hippocampal theta oscillations are travelling waves. Nature, 459, 534–539.

    Article  CAS  PubMed  Google Scholar 

  • Miles, R., Traub, R. D., & Wong, R. K. (1988). (Spread of synchronous firing in longitudinal slices from the CA3 region of the hippocampus. Journal of Neurophysiol, 60, 1481–1496.

    CAS  Google Scholar 

  • Moser, M. B., & Moser, E. I. (1998). (Distributed encoding and retrieval of spatial memory in the hippocampus. Journal of Neuroscience, 18, 7535–7542.

    CAS  PubMed  Google Scholar 

  • Nicolelis, M. A., & Ribeiro, S. (2002). (Multielectrode recordings: the next steps. Current Opinion in Neurobiology, 12, 602–606.

    Article  CAS  PubMed  Google Scholar 

  • Papatheodoropoulos, C., & Kostopoulos, G. (2002). (Spontaneous, low frequency (approximately 2–3 Hz) field activity generated in rat ventral hippocampal slices perfused with normal medium. Brain Research Bulletin, 57, 187–193.

    Article  PubMed  Google Scholar 

  • Pesaran, B., Pezaris, J. S., Sahani, M., Mitra, P. P., & Andersen, R. A. (2002). (Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nature Neuroscience, 5, 805–811.

    Article  CAS  PubMed  Google Scholar 

  • Pettersen, K. H., & Einevoll, G. T. (2008). (Amplitude variability and extracellular low-pass filtering of neuronal spikes. Biophysical Journal, 94, 784–802.

    Article  CAS  PubMed  Google Scholar 

  • Scherberger, H., Jarvis, M. R., & Andersen, R. A. (2005). (Cortical local field potential encodes movement intentions in the posterior parietal cortex. Neuron, 46, 347–354.

    Article  CAS  PubMed  Google Scholar 

  • Schwartzkroin, P. A., & Franck, J. E. (1986). (Electrophysiology of epileptic tissue: what pathologies are epileptogenic? Advances in Experimental Medicine and Biology, 203, 157–172.

    CAS  PubMed  Google Scholar 

  • Schwartzkroin, P. A., & Knowles, W. D. (1984). (Intracellular study of human epileptic cortex: in vitro maintenance of epileptiform activity? Science, 223, 709–712.

    Article  CAS  PubMed  Google Scholar 

  • Singer W (1999). Neuronal synchrony: a versatile code for the definition of relations? Neuron 24:49–65, 111–125.

    Google Scholar 

  • Skinner, F. K., Wu, C., & Zhang, L. (2001). (Phase-coupled oscillator models can predict hippocampal inhibitory synaptic connections. European Journal of Neuroscience, 13, 2183–2194.

    Article  CAS  PubMed  Google Scholar 

  • Womelsdorf, T., Fries, P., Mitra, P. P., & Desimone, R. (2006). (Gamma-band synchronization in visual cortex predicts speed of change detection. Nature, 439, 733–736.

    Article  CAS  PubMed  Google Scholar 

  • Wu, C., Luk, W. P., Gillis, J., Skinner, F., & Zhang, L. (2005). (Size does matter: generation of intrinsic network rhythms in thick mouse hippocampal slices. Journal of Neurophysiol, 93, 2302–2317.

    Article  Google Scholar 

  • Wu, C., Shen, H., Luk, W. P., & Zhang, L. (2002). (A fundamental oscillatory state of isolated rodent hippocampus. Journal of physiology, 540, 509–527.

    Article  CAS  PubMed  Google Scholar 

  • Wu, C. P., Huang, H. L., Asl, M. N., He, J. W., Gillis, J., Skinner, F. K., et al. (2006). (Spontaneous rhythmic field potentials of isolated mouse hippocampal-subicular-entorhinal cortices in vitro. Journal of physiology, 576, 457–476.

    Article  CAS  PubMed  Google Scholar 

  • Wulff, P., Ponomarenko, A. A., Bartos, M., Korotkova, T. M., Fuchs, E. C., Bahner, F., et al. (2009). (Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons. Proceedings of the National Academy of Sciences of the United States of America, 106, 3561–3566.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, Y. (1990). Atlas LE, Marks RJ (The use of cone-shape kernels for generalized time-frequency representations of nonstationary signals. I.E.E.E. transactions on acoustics, speech, and signal processing, 38, 7.

    Google Scholar 

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Acknowledgments

This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC). JAG was funded by a CIHR doctoral award, Epilepsy Canada, and the Krembil Foundation.

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Author notes

  1. Jesse A. Gillis

    Present address: Centre for High-throughput Biology (CHiBi), University of British Columbia, 183D Michael Smith Laboratories, 2185 East Mall, Vancouver, BC, V6T 1Z4, Canada

Authors and Affiliations

  1. Toronto Western Research Institute, University Health Network, Toronto, Canada

    Jesse A. Gillis, Liang Zhang & Frances K. Skinner

  2. Department of Medicine (Neurology), University of Toronto, Toronto, Canada

    Liang Zhang & Frances K. Skinner

  3. Department of Medicine Physiology, University of Toronto, Toronto, Canada

    Jesse A. Gillis & Frances K. Skinner

  4. Institute of Biomaterials and Biomedical Engineering, University of Toronto, Toronto, Canada

    Frances K. Skinner

Authors
  1. Jesse A. Gillis
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Correspondence to Jesse A. Gillis.

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Action Editor: Gaute T Einevoll, PhD

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Gillis, J.A., Zhang, L. & Skinner, F.K. Spatial coherence and stationarity of local field potentials in an isolated whole hippocampal preparation in vitro . J Comput Neurosci 29, 521–532 (2010). https://doi.org/10.1007/s10827-009-0207-x

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  • DOI: https://doi.org/10.1007/s10827-009-0207-x

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