Compensating for thalamocortical synaptic loss in Alzheimer's disease

Frontiers in Computational Neuroscience

Volumn 8, Issue JUN, 2014, Pages

  Abuhassan, Kamal ^a   Coyle, Damien ^b   Maguire, Liam ^b  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY OF ULSTER   (United Kingdom)

Author keywords

Alzheimer's disease; Connectivity loss; Electroencephalography; Synaptic compensation mechanisms; Thalamic atrophy; Thalamocortical network model; Thalamocortical oscillations

Indexed keywords

ELECTROENCEPHALOGRAPHY; ELECTROPHYSIOLOGY; FREQUENCY BANDS; MAMMALS; NEURONS; PATHOLOGY;

ALZHEIMER'S DISEASE; COMPENSATION MECHANISM; CONNECTIVITY LOSS; THALAMIC ATROPHY; THALAMO-CORTICAL NETWORK; THALAMOCORTICAL OSCILLATIONS;

NEURODEGENERATIVE DISEASES;

ALZHEIMER DISEASE; ARTICLE; DENERVATION; DISEASE ASSOCIATION; EVOKED RESPONSE; FREQUENCY MODULATION; INHIBITION (PSYCHOLOGY); NERVE CELL INHIBITION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVE STIMULATION; NERVOUS SYSTEM PARAMETERS; OSCILLATORY POTENTIAL; THALAMOCORTICAL SYNATIC LOSS; THALAMUS NUCLEUS; THALAMUS RETICULAR NUCLEUS;

EID: 84902575945     PISSN: None     EISSN: 16625188     Source Type: Journal    
DOI: 10.3389/fncom.2014.00065     Document Type: Article

References (79)

1. Abuhassan, K., Coyle, D., Belatreche, A., and Maguire, L. (2013). Compensating for synaptic loss in Alzheimer's disease. J. Comput. Neurosci. 36, 19-37. doi: 10.1007/s10827-013-0462-8
2. Abuhassan, K., Coyle, D., and Maguire, L. P. (2012). Investigating the neural correlates of pathological cortical networks in Alzheimer's disease using heterogeneous neuronal models. IEEE Trans. Biomed. Eng. 59, 890-896. doi: 10.1109/TBME.2011.2181843
3. Agmon, A., and Connors, B. W. (1992). Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex. J. Neurosci. 12, 319-329.
4. Bazhenov, M., Timofeev, I., Steriade, M., and Sejnowski, T. (2002). Model of tha-lamocortical slow-wave sleep oscillations and transitions to activated states. J. Neurosci. 22, 8691-8704.
5. Benarroch, E. E. (2012). GABAB receptors: structure, functions, and clinical implications. Neurology 78, 578-584. doi: 10.1212/WNL.0b013e318247cd03
6. Bhattacharya, B. S., Coyle, D., and Maguire, L. (2011). A thalamo-cortico-thalamic neural mass model to study alpha rhythms in Alzheimer's disease. Neural Netw. 24, 631-645. doi: 10.1016/j.neunet.2011.02.009
7. Bhattacharya, B. S., Coyle, D., and Maguire, L. (2012). Assessing alpha band event-related synchronisation/desynchronisation using a bio-inspired computational model. J. Universal Comput. Sci. 18, 1888-1904. doi: 10.3217/jucs-018-13-1888
8. Binzegger, T., Douglas, R. J., and Martin, K. A. C. (2004). A quantitative map of the circuit of cat primary visual cortex. J. Neurosci. 24, 8441-8453. doi: 10.1523/JNEUROSCI.1400-04.2004
9. Braitenberg, V., and Schüz, A. (1998). Cortex: Statistics and Geometry of Neuronal Connectivity. Berlin: Springer. doi: 10.1007/978-3-662-03733-1
10. Castro-Alamancos, M. A., and Calcagnotto, M. E. (1999). Presynaptic long-term potentiation in corticothalamic synapses. J. Neurosci. 19, 9090-9097.
11. Cho, H., Seo, S. W., Kim, J.-H., Kim, C., Ye, B. S., Kim, G. H., et al. (2013). Changes in subcortical structures in early- versus late-onset Alzheimer's disease. Neurobiol. Aging 34, 1740-1747. doi: 10.1016/j.neurobiolaging.2013.01.001
12. Contreras, D., Destexhe, A., Sejnowski, T. J., and Steriade, M. (1996). Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback. Science (New York, NY) 274, 771-774. doi: 10.1126/science.274.5288.771
13. Coyle, D., Prasad, G., and McGinnity, T. M. (2005). A time-frequency approach to feature extraction for a brain-computer interface with a comparative analysis of performance measures. EURASIP J. Adv. Signal Process. 2005, 3141-3151. doi: 10.1155/ASP.2005.3141
14. De Jong, L. W., Van der Hiele, K., Veer, I. M., Houwing, J. J., Westendorp, R. G. J., Bollen, E. L. E. M., et al. (2008). Strongly reduced volumes of putamen and tha-lamus in Alzheimer's disease: an MRI study. Brain 131, 3277-3285. doi: 10.1093/brain/awn278
15. Destexhe, A. (2000). Modelling corticothalamic feedback and the gating of the tha-lamus by the cerebral cortex. J. Physiol. Paris 94, 391-410. doi: 10.1016/S0928-4257(00)01093-7
16. Durka, P. J., Zygierewicz, J., Klekowicz, H., Ginter, J., and Blinowska, K. J. (2004a). ERD/ERS Software Tool. Available online at: http://eeg.pl/Members/durka/dataset.2008-02-12.5871220409
17. Durka, P. J., Zygierewicz, J., Klekowicz, H., Ginter, J., and Blinowska, K. J. (2004b). On the statistical significance of event-related EEG desynchronization and synchronization in the time-frequency plane. IEEE Trans. Biomed. Eng. 51, 1167-1175. doi: 10.1109/TBME.2004.827341
18. Fröhlich, F., Bazhenov, M., and Sejnowski, T. J. (2008). Pathological effect of homeostatic synaptic scaling on network dynamics in diseases of the cortex. J. Neurosci. 28, 1709-1720. doi: 10.1523/JNEUROSCI.4263-07.2008
19. Gentet, L. J., and Ulrich, D. (2004). Electrophysiological characterization of synaptic connections between layer VI cortical cells and neurons of the nucleus reticularis thalami in juvenile rats. Eur. J. Neurosci. 19, 625-633. doi: 10.1111/j.1460-9568.2004.03168.x
20. Gupta, A. (2000). Organizing principles for a diversity of GABAergic interneu-rons and synapses in the neocortex. Science 287, 273-278. doi: 10.1126/sci-ence.287.5451.273
21. Herman, P., Prasad, G., McGinnity, T. M., and Coyle, D. (2008). Comparative analysis of spectral approaches to feature extraction for EEG-based motor imagery classification. IEEE Trans. Neural Syst. Rehabil. Eng. 16, 317-326. doi: 10.1109/TNSRE.2008.926694
22. Holtmaat, A., and Svoboda, K. (2009). Experience-dependent structural synap-tic plasticity in the mammalian brain. Nat. Rev. Neurosci. 10, 647-658. doi: 10.1038/nrn2699
23. Hughes, S. W., and Crunelli, V. (2005). Thalamic mechanisms of EEG alpha rhythms and their pathological implications. Neuroscientist 11, 357-372. doi: 10.1177/1073858405277450
24. Izhikevich, E. M. (2007). Dynamical systems in neuroscience: the geometry of excitability and bursting. Dyn. Syst. 25, 441.
25. Izhikevich, E. M., and Edelman, G. M. (2008). Large-scale model of mammalian thalamocortical systems. Proc. Natl. Acad. Sci. U.S.A. 105, 3593-3598. doi: 10.1073/pnas.0712231105
26. Izhikevich, E. M., Gally, J. A., and Edelman, G. M. (2004). Spike-timing dynamics of neuronal groups. Cereb. Cortex 14, 933-944. doi: 10.1093/cercor/bhh053
27. Jelic, V. (2000). Quantitative electroencephalography in mild cognitive impairment: longitudinal changes and possible prediction of Alzheimer's disease. Neurobiol. Aging. 21, 533-540. doi: 10.1016/S0197-4580(00)00153-6
28. Jelles, B., Scheltens, P., Van der Flier, W. M., Jonkman, E. J., Da Silva, F. H. L., and Stam, C. J. (2008). Global dynamical analysis of the EEG in Alzheimer's disease: frequency-specific changes of functional interactions. Clin. Neurophysiol. 119, 837-841. doi: 10.1016/j.clinph.2007.12.002
29. Jeong, J. (2004). EEG dynamics in patients with Alzheimer's disease. Clin. Neurophysiol. 115, 1490-1505. doi: 10.1016/j.clinph.2004.01.001
30. Jin, K., Peel, A. L., Mao, X. O., Xie, L., Cottrell, B. A., Henshall, D. C., et al. (2004). Increased hippocampal neurogenesis in Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 101, 343-347. doi: 10.1073/pnas.2634794100
31. Johnson, M. D., and Ojemann, G. A. (2000). The role of the human thalamus in language and memory: evidence from electrophysiological studies. Brain Cogn. 42, 218-230. doi: 10.1006/brcg.1999.1101
32. Jones, E. G. (1985). The Thalamus. 1st Edn. New York, NY: Plenum Press. doi: 10.1007/978-1-4615-1749-8
33. Jones, E. G. (2002). Thalamic circuitry and thalamocortical synchrony. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 357, 1659-1673. doi: 10.1098/rstb.2002.1168
34. Kirkcaldie, M. (2012). "Neocortex," in The Mouse Nervous System, eds C. Watson, G. Paxinos, and L. Puelles (London: Academic Press), 52-94. doi: 10.1016/B978-0-12-369497-3.10004-4
35. Koenig, T., Prichep, L., Dierks, T., Hubl, D., Wahlund, L. O., John, E. R., et al. (2005). Decreased EEG synchronization in Alzheimer's disease and mild cognitive impairment. Neurobiol. Aging 26, 165-171. doi: 10.1016/j.neurobiolaging.2004.03.008
36. Landisman, C. E., Long, M. A., Beierlein, M., Deans, M. R., Paul, D. L., and Connors, B. W. (2002). Electrical synapses in the thalamic reticular nucleus. J. Neurosci. 22, 1002-1009.
37. Leuba, G., Savioz, A., Vernay, A., Carnal, B., Kraftsik, R., Tardif, E., et al. (2008). Differential changes in synaptic proteins in the Alzheimer frontal cortex with marked increase in PSD-95 postsynaptic protein. J. Alzheimers Dis. 15, 139-151.
38. Li, X., Coyle, D., Maguire, L., Watson, D. R., and McGinnity, T. M. (2011). Gray matter concentration and effective connectivity changes in Alzheimer's disease: a longitudinal structural MRI study. Neuroradiology 53, 733-748. doi: 10.1007/s00234-010-0795-1
39. Manshanden, I., De Munck, J. C., Simon, N. R., and Lopes da Silva, F. H. (2002). Source localization of MEG sleep spindles and the relation to sources of alpha band rhythms. Clin. Neurophysiol. 113, 1937-1947. doi: 10.1016/S1388-2457(02)00304-8
40. Markram, H., Wang, Y., and Tsodyks, M. (1998). Differential signaling via the same axon of neocortical pyramidal neurons. Proc. Natl. Acad. Sci. U.S.A. 95, 5323-5328. doi: 10.1073/pnas.95.9.5323
41. Mayer, J., Schuster, H. G., Claussen, J. C., and Mölle, M. (2007). Corticothalamic projections control synchronization in locally coupled bistable thalamic oscillators. Phys. Rev. Lett. 99, 068102. doi: 10.1103/PhysRevLett.99.068102
42. Moretti, D. V., Babiloni, C., Binetti, G., Cassetta, E., Dal Forno, G., Ferreric, F., et al. (2004). Individual analysis of EEG frequency and band power in mild Alzheimer's disease. Clin. Neurophysiol. 115, 299-308. doi: 10.1016/S1388-2457(03)00345-6
43. Nuwer, M. R., Comi, G., Emerson, R., Fuglsang-Frederiksen, A., Guérit, J. M., Hinrichs, H., et al. (1999). IFCN standards for digital recording of clinical EEG. International Federation of Clinical Neurophysiology. Electroencephalogr. Clin. Neurophysiol. 52, 11-14.
44. O'Dwyer, L., Lamberton, F., Matura, S., Tanner, C., Scheibe, M., Miller, J., et al. (2012). Reduced hippocampal volume in healthy young ApoE4 carriers: an MRI study. PLoS ONE 7:e48895. doi: 10.1371/journal.pone.0048895.
45. Park, Y.-M., Che, H.-J., Im, C.-H., Jung, H.-T., Bae, S.-M., and Lee, S.-H. (2008). Decreased EEG synchronization and its correlation with symptom severity in Alzheimer's disease. Neurosci. Res. 62, 112-117. doi: 10.1016/j.neures.2008.06.009
46. Paz, J. T., Christian, C. A., Parada, I., Prince, D. A., and Huguenard, J. R. (2010). Focal cortical infarcts alter intrinsic excitability and synaptic excitation in the reticular thalamic nucleus. J. Neurosci. 30, 5465-5479. doi: 10.1523/JNEUROSCI.5083-09.2010
47. Pedro, T., Weiler, M., Yasuda, C. L., D'Abreu, A., Damasceno, B. P., Cendes, F., et al. (2012). Volumetric brain changes in thalamus, corpus callosum and medial temporal structures: mild Alzheimer's disease compared with amnestic mild cognitive impairment. Dement. Geriatr. Cogn. Disord. 34, 149-155. doi: 10.1159/000342118
48. Pfurtscheller, G., and Aranibar, A. (1977). Event-related cortical desyn-chronization detected by power measurements of scalp EEG. Electroencephalogr. Clin. Neurophysiol. 42, 817-826. doi: 10.1016/0013-4694(77)90235-8
49. Pfurtscheller, G., and Lopes da Silva, F. H. (1999). Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin. Neurophysiol. 110, 1842-1857. doi: 10.1016/S1388-2457(99)00141-8
50. Pons, A. J., Cantero, J. L., Atienza, M., and Garcia-Ojalvo, J. (2010). Relating structural and functional anomalous connectivity in the aging brain via neural mass modeling. Neuroimage 52, 848-861. doi: 10.1016/j.neuroimage.2009.12.105
51. Prasad, G., Herman, P., Coyle, D., McDonough, S., and Crosbie, J. (2010). Applying a brain-computer interface to support motor imagery practice in people with stroke for upper limb recovery: a feasibility study. J. Neuroeng. Rehabil. 7, 60. doi: 10.1186/1743-0003-7-60
52. Qi, Z., Wu, X., Wang, Z., Zhang, N., Dong, H., Yao, L., et al. (2010). Impairment and compensation coexist in amnestic MCI default mode network. Neuroimage 50, 48-55. doi: 10.1016/j.neuroimage.2009.12.025
53. Ryan, N. S., Keihaninejad, S., Shakespeare, T. J., Lehmann, M., Crutch, S. J., Malone, I. B., et al. (2013). Magnetic resonance imaging evidence for presymptomatic change in thalamus and caudate in familial Alzheimer's disease. Brain 136, 1399-1414. doi: 10.1093/brain/awt065
54. Savioz, A., Leuba, G., Vallet, P. G., and Walzer, C. (2009). Contribution of neural networks to Alzheimer disease's progression. Brain Res. Bull. 80, 309-314. doi: 10.1016/j.brainresbull.2009.06.006
55. Scheff, S. W. (2003). Reactive synaptogenesis in aging and Alzheimer's disease: lessons learned in the Cotman laboratory. Neurochem. Res. 28, 1625-1630. doi: 10.1023/A:1026048619220
56. Scheff, S. W., and Price, D. A. (1993). Synapse loss in the temporal lobe in Alzheimer's disease. Ann. Neurol. 33, 190-199. doi: 10.1002/ana.410330209
57. Sherman, S. M. (2001). A wake-up call from the thalamus. Nat. Neurosci. 4, 344-346. doi: 10.1038/85973
58. Small, D. H. (2004). Mechanisms of synaptic homeostasis in Alzheimer's disease. Curr. Alzheimer Res. 1, 27-32. doi: 10.2174/1567205043480573
59. Sohal, V. S., Huntsman, M. M., and Huguenard, J. R. (2000). Reciprocal inhibitory connections regulate the spatiotemporal properties of intrathalamic oscillations. J. Neurosci. 20, 1735-1745.
60. Stellwagen, D., and Malenka, R. C. (2006). Synaptic scaling mediated by glial TNF-alpha. Nature 440, 1054-1059. doi: 10.1038/nature04671
61. Steriade, M. (2005). Sleep, epilepsy and thalamic reticular inhibitory neurons. Trends Neurosci. 28, 317-324. doi: 10.1016/j.tins.2005.03.007
62. Steriade, M., Jones, E. G., and Llinás, R. R. (1990). Thalamic oscillations and signaling. New York, NY, US: Wiley.
63. Steriade, M., Nuñez, A., and Amzica, F. (1993). Intracellular analysis of relations between the slow (< 1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J. Neurosci. 13, 3266-3283.
64. Supekar, K., Menon, V., Rubin, D., Musen, M., and Greicius, M. D. (2008). Network analysis of intrinsic functional brain connectivity in Alzheimer's disease. PLoS Comput. Biol. 4:e1000100. doi: 10.1371/journal.pcbi.1000100
65. Swadlow, H. A. (1994). Efferent neurons and suspected interneurons in motor cortex of the awake rabbit: axonal properties, sensory receptive fields, and subthreshold synaptic inputs. J. Neurophysiol. 71, 437-453.
66. Timofeev, I., and Steriade, M. (1996). Low-frequency rhythms in the thalamus of intact-cortex and decorticated cats. J. Neurophysiol. 76, 4152-4168.
67. Traub, R. D., Contreras, D., Cunningham, M. O., Murray, H., LeBeau, F. E. N., Roopun, A., et al. (2005). Single-column thalamocortical network model exhibiting gamma oscillations, sleep spindles, and epileptogenic bursts. J. Neurophysiol. 93, 2194-2232. doi: 10.1152/jn.00983.2004
68. Turrigiano, G. (2011). Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. Annu. Rev. Neurosci. 34, 89-103. doi: 10.1146/annurev-neuro-060909-153238
69. Turrigiano, G. (2012). Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harb. Perspect. Biol. 4:a005736. doi: 10.1101/cshperspect.a005736
70. Uylings, H. B. M., and De Brabander, J. M. (2002). Neuronal changes in normal human aging and Alzheimer's disease. Brain Cogn. 49, 268-276. doi: 10.1006/brcg.2001.1500
71. Van der Werf, Y. D., Scheltens, P., Lindeboom, J., Witter, M. P., Uylings, H. B. M., and Jolles, J. (2003). Deficits of memory, executive functioning and attention following infarction in the thalamus; a study of 22 cases with localised lesions. Neuropsychologia 41, 1330-1344. doi: 10.1016/S0028-3932(03)00059-9
72. Wang, Z., Jia, X., Liang, P., Qi, Z., Yang, Y., Zhou, W., et al. (2012). Changes in thalamus connectivity in mild cognitive impairment: evidence from resting state fMRI. Eur. J. Radiol. 81, 277-285. doi: 10.1016/j.ejrad.2010.12.044
73. Waxman, S. G., and Bennett, M., V (1972). Relative conduction velocities of small myelinated and non-myelinated fibres in the central nervous system. Nat. New Biol. 238, 217-219. doi: 10.1038/newbio238217a0
74. Woolfolk, A. (2011). Educational Psychology. 11th Edn. Columbus, OH: Pearson/Allyn & Bacon.
75. Yazawa, S., Kawasaki, S., Kanemaru, A., Kuratsuwa, Y., Yabuoshi, R., and Ohi, T. (2001). Bilateral paramedian thalamo-midbrain infarction showing electroen-cephalographic alpha activity. Intern. Med. 40, 443-448. doi: 10.2169/inter-nalmedicine.40.443
76. Zarei, M., Patenaude, B., Damoiseaux, J., Morgese, C., Smith, S., Matthews, P. M., et al. (2010). Combining shape and connectivity analysis: an MRI study of thalamic degeneration in Alzheimer's disease. Neuroimage 49, 1-8. doi: 10.1016/j.neuroimage.2009.09.001
77. Zhang, S. J., Huguenard, J. R., and Prince, D. A. (1997). GABAA receptor-mediated Cl- currents in rat thalamic reticular and relay neurons. J. Neurophysiol. 78, 2280-2286.
78. Zhao, X., Liu, Y., Wang, X., Liu, B., Xi, Q., Guo, Q., et al. (2012). Disrupted small-world brain networks in moderate Alzheimer's disease: a resting-state FMRI study. PLoS ONE 7:e33540. doi: 10.1371/journal.pone.0033540
79. Zikopoulos, B., and Barbas, H. (2006). Prefrontal projections to the thalamic reticular nucleus form a unique circuit for attentional mechanisms. J. Neurosci. 26, 7348-7361. doi: 10.1523/JNEUROSCI.5511-05.2006