Abstract
Alterations in oscillatory brain activity are strongly correlated with cognitive performance in various physiological rhythms. The present study investigated whether the directionality of neural information flow (NIF) could be used to characterize the synaptic plasticity in thalamocortical (TC) pathway, and examined which frequency field oscillations were mostly related to the cognitive deficiency in depression. Two novel algorithms were employed to determine the coupling interaction between the LD thalamus and medial prefrontal cortex (mPFC) in five frequency bands, using the phase signals of local field potentials (LFP) in these two regions. The results showed that the power of neural activity in mPFC was increased in delta, theta and beta frequency bands in depression. However, the nonlinear characteristics of LFP activity were weakened in depression by means of sample entropy measurements. In the analysis of phase dynamics, the phase synchronization values were reduced in theta rhythm in stressed rats. Importantly, the coupling direction index d and the unidirectional influence from LD thalamus to mPFC were significantly reduced at the theta rhythm in rats in depression, and increased after memantine treatment, which were associated with the LTP alterations and cognitive impairment in our previous report. Moreover, the fact that the reduced entropy value was only found in mPFC might implicate postsynaptic effect involved in synaptic plasticity alteration in the depression model. The results suggest that the effects of depression on cognitive deficits are mediated via profound alterations in information flow in the TC pathway, and the directional index at theta rhythm could be used as a measurement of synaptic plasticity.






Similar content being viewed by others
References
Başar, E., & Güntekin, B. (2008). A review of brain oscillations in cognitive disorders and the role of neurotransmitters. Brain Research, 1235, 172–193.
Başar-Eroglu, C., Başar, E., Demiralp, T., & Schürmann, M. (1992). P300-response: possible psychophysiological correlates in delta and theta frequency channels. A review. International Journal of Psychophysiology, 13(2), 161–179.
Bauer, L. O., & Hesselbrock, V. M. (1993). EEG, autonomic and subjective correlates of the risk for alcoholism. Journal of Studies on Alcohol, 54(5), 577–589.
Bondi, C. O., Rodriguez, G., Gould, G. G., Frazer, A., & Morilak, D. A. (2007). Chronic unpredictable stress induces a cognitive deficit and anxiety-like behavior in rats that is prevented by chronic antidepressant drug treatment. Neuropsychopharmacology, 33(2), 320–331.
Brea, J., Russell, D. F., & Neiman, A. B. (2006). Measuring direction in the coupling of biological oscillators: a case study for electroreceptors of paddlefish. Chaos: An Interdisciplinary Journal of Nonlinear Science, 16(2), 026111.
Bruno, R. M., & Sakmann, B. (2006). Cortex is driven by weak but synchronously active thalamocortical synapses. Science, 312(5780), 1622–1627.
Buzsaki, G. (2002). Theta oscillations in the hippocampus. Neuron, 33(3), 325–340.
Buzsaki, G., & Draguhn, A. (2004). Neuronal oscillations in cortical networks. Science, 304(5679), 1926–1929. doi:10.1126/science.1099745.
Colgin, L. L., & Moser, E. I. (2010). Gamma oscillations in the hippocampus. Physiology (Bethesda, Md.), 25(5), 319–329. doi:10.1152/physiol.00021.2010.
Csicsvari, J., Jamieson, B., Wise, K. D., & Buzsaki, G. (2003). Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron, 37(2), 311–322.
Dalley, J. W., Cardinal, R. N., & Robbins, T. W. (2004). Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neuroscience and Biobehavioral Reviews, 28(7), 771–784.
Davis, K. L., Charney, D. S., Coyle, J. T., & Nemeroff, C. B. (2002). Neuropsychopharmacology: The fbifth generation of progress. Philadelphia: Lippincott Williams & Wilkins.
Düzel, E., Penny, W. D., & Burgess, N. (2010). Brain oscillations and memory. Current Opinion in Neurobiology, 20(2), 143–149. doi:10.1016/j.conb.2010.01.004.
Ford, J. M., Roach, B. J., Hoffman, R. S., & Mathalon, D. H. (2008). The dependence of P300 amplitude on gamma synchrony breaks down in schizophrenia. Brain Research, 1235, 133–142.
Gallinat, J., Kunz, D., Senkowski, D., Kienast, T., Seifert, F., Schubert, F., et al. (2006). Hippocampal glutamate concentration predicts cerebral theta oscillations during cognitive processing. Psychopharmacology, 187(1), 103–111.
Goldman-Rakic, P. S. (1988). Topography of cognition: parallel distributed networks in primate association cortex. Annual Review of Neuroscience, 11(1), 137–156.
Grin-Yatsenko, V. A., Baas, I., Ponomarev, V. A., & Kropotov, J. D. (2010). Independent component approach to the analysis of EEG recordings at early stages of depressive disorders. Clinical Neurophysiology, 121(3), 281–289.
Izaki, Y., & Akema, T. (2008). Gamma-band power elevation of prefrontal local field potential after posterior dorsal hippocampus-prefrontal long-term potentiation induction in anesthetized rats. Experimental Brain Research, 184(2), 249–253. doi:10.1007/s00221-007-1098-6.
Izaki, Y., Fujiwara, S. E., & Akema, T. (2008). Rat prefrontal response and prestimulation local field potential power in vivo. Neuroreport, 19(2), 255–258. doi:10.1097/WNR.0b013e3282f4cb3a.
Katz, R. J. (1982). Animal model of depression: pharmacological sensitivity of a hedonic deficit. Pharmacology Biochemistry and Behavior, 16(6), 965–968.
Kirk, I. J., & Mackay, J. C. (2003). The role of theta-range oscillations in synchronising and integrating activity in distributed mnemonic networks. Cortex, 39(4–5), 993–1008.
Malenka, R. C., & Bear, M. F. (2004). LTP and LTD: an embarrassment of riches. Neuron, 44(1), 5–21. doi:10.1016/j.neuron.2004.09.012.
McKInney, W. T. (2003). Animal models of neuropsychiatric disorders. Handbook of medical psychiatry, 1.
Munk, M. H. J., Roelfsema, P. R., Konig, P., Engel, A. K., & Singer, W. (1996). Role of reticular activation in the modulation of intracortical synchronization. Science(Washington), 272(5259), 271–271.
Neiman, A. B., & Russell, D. F. (2004). Two distinct types of noisy oscillators in electroreceptors of paddlefish. Journal of Neurophysiology, 92(1), 492–509.
Özerdem, A., Kocaaslan, S., Tunca, Z., & Başar, E. (2007). Effect of valproate on oscillatory delta frequency responses to visual stimuli in a group euthymic bipolar patients in comparison to healthy controls. Biological Psychiatry, 61, 1S–266S.
Özerdem, A., Güntekin, B., Tunca, Z., & Başar, E. (2008). Brain oscillatory responses in patients with bipolar disorder manic episode before and after valproate treatment. Brain Research, 1235, 98–108.
Paluš, M., & Stefanovska, A. (2003). Direction of coupling from phases of interacting oscillators: an information-theoretic approach. Physical Review. E, Statistical, Nonlinear, and Soft Matter Physics, 67(5 Pt 2), 055201.
Paluš, M., Komarek, V., Hrncir, Z., & Sterbova, K. (2001). Synchronization as adjustment of information rates: detection from bivariate time series. Physical Review. E, Statistical, Nonlinear, and Soft Matter Physics, 63(4 Pt 2), 046211.
Quan, M. N., Tian, Y. T., Xu, K. H., Zhang, T., & Yang, Z. (2010). Post weaning social isolation influences spatial cognition, prefrontal cortical synaptic plasticity and hippocampal potassium ion channels in Wistar rats. Neuroscience, 169(1), 214–222. doi:10.1016/j.neuroscience.2010.04.048.
Quan, M. N., Zhang, N., Wang, Y. Y., Zhang, T., & Yang, Z. (2011a). Possible antidepressant effects and mechanisms of memantine in behaviors and synaptic plasticity of a depression rat model. Neuroscience, 182, 88–97. doi:10.1016/j.neuroscience.2011.03.026.
Quan, M. N., Zheng, C. G., Zhang, N., Han, D. D., Tian, Y. T., Zhang, T., et al. (2011b). Impairments of behavior, information flow between thalamus and cortex, and prefrontal cortical synaptic plasticity in an animal model of depression. Brain Research Bulletin, 85(3–4), 109–116. doi:10.1016/j.brainresbull.2011.03.002.
Rosenblum, M. G., & Pikovsky, A. S. (2001). Detecting direction of coupling in interacting oscillators. Physical Review E, 64(4), 45202.
Rosenblum, M. G., Cimponeriu, L., Bezerianos, A., Patzak, A., & Mrowka, R. (2002). Identification of coupling direction: application to cardiorespiratory interaction. Physical Review. E, Statistical, Nonlinear, and Soft Matter Physics, 65(4 Pt 1), 041909.
Smirnov, D. A., & Andrzejak, R. G. (2005). Detection of weak directional coupling: phase-dynamics approach versus state-space approach. Physical Review E, 71(3), 36207.
Tariot, P. N., Farlow, M. R., Grossberg, G. T., Graham, S. M., McDonald, S., & Gergel, I. (2004). Memantine treatment in patients with moderate to severe Alzheimer disease already receiving donepezil: a randomized controlled trial. JAMA, 291(3), 317–324. doi:10.1001/jama.291.3.317.
Wagner, T., Axmacher, N., Lehnertz, K., Elger, C. E., & Fell, J. (2009). Sleep-dependent directional coupling between human neocortex and hippocampus. Cortex, 46(2), 256–263. doi:10.1016/j.cortex.2009.05.012.
Wallace, D. L., Han, M. H., Graham, D. L., Green, T. A., Vialou, V., Iniguez, S. D., et al. (2009). CREB regulation of nucleus accumbens excitability mediates social isolation¨Cinduced behavioral deficits. Nature Neuroscience, 12(2), 200–209.
Welsh, R. C., Chen, A. C., & Taylor, S. F. (2008). Low-frequency BOLD fluctuations demonstrate altered thalamocortical connectivity in schizophrenia. Schizophrenia Bulletin, 36(4), 713–722.
Willner, P. (1997). Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology, 134(4), 319–329.
Willner, P. (2005). Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology, 52(2), 90–110.
Yang, Z., Zhang, T., & Coote, J. (2002). Synchrony analysis between blood pressure and sympathetic nerve signal inhibited by atrial receptor stimulation in Wistar rats. Experimental Physiology, 87(4), 461–468.
Yener, G., Güntekin, B., Öniz, A., & Başar, E. (2007). Increased frontal phase-locking of event-related theta oscillations in Alzheimer patients treated with cholinesterase inhibitors. International Journal of Psychophysiology, 64(1), 46–52.
Zhang, T., & Turner, D. (2001). A visuomotor reaction time task increases the irregularity and complexity of inspiratory airflow pattern in man. Neuroscience Letters, 297(1), 41–44.
Zhang, T., Yang, Z., & Coote, J. (2007). Cross-sample entropy statistic as a measure of complexity and regularity of renal sympathetic nerve activity in the rat. Experimental Physiology, 92(4), 659–669.
Acknowledgements
This work was supported by grants from the National Natural Science Foundation of China (31171053 and 30870827) and Tianjin research program of application foundation and advanced technology (12JCZDJC22300).
Author information
Authors and Affiliations
Corresponding author
Additional information
Action Editor: Simon R. Schultz
Rights and permissions
About this article
Cite this article
Zheng, C., Quan, M. & Zhang, T. Decreased thalamo-cortical connectivity by alteration of neural information flow in theta oscillation in depression-model rats. J Comput Neurosci 33, 547–558 (2012). https://doi.org/10.1007/s10827-012-0400-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10827-012-0400-1
Keywords
Profiles
- Chenguang Zheng View author profile