Impact of cognitive stimulation on ripples within human epileptic and non-epileptic hippocampus

. 2015 Jul 25 ; 16 () : 47. [epub] 20150725

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid26205426
Odkazy

PubMed 26205426
PubMed Central PMC4513957
DOI 10.1186/s12868-015-0184-0
PII: 10.1186/s12868-015-0184-0
Knihovny.cz E-zdroje

BACKGROUND: Until now there has been no way of distinguishing between physiological and epileptic hippocampal ripples in intracranial recordings. In the present study we addressed this by investigating the effect of cognitive stimulation on interictal high frequency oscillations in the ripple range (80-250 Hz) within epileptic (EH) and non-epileptic hippocampus (NH). METHODS: We analyzed depth EEG recordings in 10 patients with intractable epilepsy, in whom hippocampal activity was recorded initially during quiet wakefulness and subsequently during a simple cognitive task. Using automated detection of ripples based on amplitude of the power envelope, we analyzed ripple rate (RR) in the cognitive and resting period, within EH and NH. RESULTS: Compared to quiet wakefulness we observed a significant reduction of RR during cognitive stimulation in EH, while it remained statistically marginal in NH. Further, we investigated the direct impact of cognitive stimuli on ripples (i.e. immediately post-stimulus), which showed a transient statistically significant suppression of ripples in the first second after stimuli onset in NH only. CONCLUSION: Our results point to a differential reactivity of ripples within EH and NH to cognitive stimulation.

Zobrazit více v PubMed

Buzsaki G, Horvath Z, Urioste R, Hetke J, Wise K. High-frequency network oscillation in the hippocampus. Science (80) 1992;256:1025–1027. doi: 10.1126/science.1589772. PubMed DOI

Bragin A, Engel J, Wilson CL, Fried I, Buzsaki G. High-frequency oscillations in human brain. Hippocampus. 1999;9:137–142. doi: 10.1002/(SICI)1098-1063(1999)9:2<137::AID-HIPO5>3.0.CO;2-0. PubMed DOI

Staba RJ, Wilson CL, Bragin A, Fried I, Engel J. Quantitative analysis of high-frequency oscillations (80–500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. J Neurophysiol. 2002;88:1743–1752. PubMed

Engel J, Bragin A, Staba R, Mody I. High-frequency oscillations: what is normal and what is not? Epilepsia. 2009;50:598–604. doi: 10.1111/j.1528-1167.2008.01917.x. PubMed DOI

Engel J, da Silva FL. High-frequency oscillations—where we are and where we need to go. Prog Neurobiol. 2012;98:316–318. doi: 10.1016/j.pneurobio.2012.02.001. PubMed DOI PMC

Buzsaki G, da Silva FL. High frequency oscillations in the intact brain. Prog Neurobiol. 2012;98:241–249. doi: 10.1016/j.pneurobio.2012.02.004. PubMed DOI PMC

Axmacher N, Elger CE, Fell J. Ripples in the medial temporal lobe are relevant for human memory consolidation. Brain. 2008;131:1806–1817. doi: 10.1093/brain/awn103. PubMed DOI

Carr MF, Jadhav SP, Frank LM. Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat Neurosci. 2011;14:147–153. doi: 10.1038/nn.2732. PubMed DOI PMC

Girardeau G, Zugaro M. Hippocampal ripples and memory consolidation. Curr Opin Neurobiol. 2011;21:452–459. doi: 10.1016/j.conb.2011.02.005. PubMed DOI

Lachaux J-P, Axmacher N, Mormann F, Halgren E, Crone NE. High-frequency neural activity and human cognition: {Past}, present and possible future of intracranial {EEG research} Prog Neurobiol. 2012;98:279–301. doi: 10.1016/j.pneurobio.2012.06.008. PubMed DOI PMC

Buzsaki G. Hippocampal sharp waves—their origin and significance. Brain Res. 1986;398:242–252. doi: 10.1016/0006-8993(86)91483-6. PubMed DOI

Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G. Gamma (40–100-Hz) oscillation in the hippocampus of the behaving rat. J Neurosci. 1995;15:47–60. PubMed PMC

Bragin A, Wilson CL, Almajano J, Mody I, Engel T. High-frequency oscillations after status epilepticus: epileptogenesis and seizure genesis. Epilepsia. 2004;45:1017–1023. doi: 10.1111/j.0013-9580.2004.17004.x. PubMed DOI

Jacobs J, Staba R, Asano E, Otsubo H, Wu JY, Zijlmans M, et al. High-frequency oscillations (HFOs) in clinical epilepsy. Prog Neurobiol. 2012;98:302–315. doi: 10.1016/j.pneurobio.2012.03.001. PubMed DOI PMC

Crepon B, Navarro V, Hasboun D, Clemenceau S, Martinerie J, Baulac M, et al. Mapping interictal oscillations greater than 200 Hz recorded with intracranial macroelectrodes in human epilepsy. Brain. 2010;133:33–45. doi: 10.1093/brain/awp277. PubMed DOI

Talairach J (1967) Atlas D’anatomie Stéréotaxique Du Télencéphale; Études Anatomo-Radiologiques, Par. J. Talairach [et Al.]. Masson, Paris

Worrell GA, Gardner AB, Stead SM, Hu S, Goerss S, Cascino GJ, et al. High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macroelectrode recordings. Brain. 2008;131:928–937. doi: 10.1093/brain/awn006. PubMed DOI PMC

Ibarz JM, Foffani G, Cid E, Inostroza M, de la Prida L. Emergent dynamics of fast ripples in the epileptic hippocampus. J Neurosci. 2010;30:16249–16261. doi: 10.1523/JNEUROSCI.3357-10.2010. PubMed DOI PMC

Bragin A, Benassi SK, Kheiri F, Engel J. Further evidence that pathologic high-frequency oscillations are bursts of population spikes derived from recordings of identified cells in dentate gyrus. Epilepsia. 2011;52:45–52. doi: 10.1111/j.1528-1167.2010.02896.x. PubMed DOI PMC

Maier N, Tejero-Cantero A, Dorrn AL, Winterer J, Beed PS, Morris G, et al. Coherent phasic excitation during hippocampal ripples. Neuron. 2011;72:137–152. doi: 10.1016/j.neuron.2011.08.016. PubMed DOI

Alvarado-Rojas C, Huberfeld G, Baulac M, Clemenceau S, Charpier S, Miles R, et al. Different mechanisms of ripple-like oscillations in the human epileptic subiculum. Ann Neurol. 2015;77:281–290. doi: 10.1002/ana.24324. PubMed DOI PMC

Gulyás AI, Freund TT (2015) Generation of physiological and pathological high frequency oscillations: the role of perisomatic inhibition in sharp-wave ripple and interictal spike generation. Curr Opin Neurobiol 31:26–32. [{SI}: {Brain} Rhythms and Dynamic Coordination] PubMed

Csicsvari J, Hirase H, Mamiya A, Buzsaki G. Ensemble patterns of hippocampal CA3–CA1 neurons during sharp wave-associated population events. Neuron. 2000;28:585–594. doi: 10.1016/S0896-6273(00)00135-5. PubMed DOI

Klausberger T, Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science (80) 2008;321:53–57. doi: 10.1126/science.1149381. PubMed DOI PMC

Kudrimoti HS, Barnes CA, McNaughton BL. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci. 1999;19:4090–4101. PubMed PMC

O’Neill J, Senior T, Csicsvari J. Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron. 2006;49:143–155. doi: 10.1016/j.neuron.2005.10.037. PubMed DOI

Davidson TJ, Kloosterman F, Wilson MA. Hippocampal replay of extended experience. Neuron. 2009;63:497–507. doi: 10.1016/j.neuron.2009.07.027. PubMed DOI PMC

Gupta AS, van der Meer MAA, Touretzky DS, Redish AD. Hippocampal replay is not a simple function of experience. Neuron. 2010;65:695–705. doi: 10.1016/j.neuron.2010.01.034. PubMed DOI PMC

Skaggs WE, McNaughton BL, Permenter M, Archibeque M, Vogt J, Amaral DG, et al. EEG sharp waves and sparse ensemble unit activity in the Macaque hippocampus. J Neurophysiol. 2007;98:898–910. doi: 10.1152/jn.00401.2007. PubMed DOI

Van Quyen M, Le Bragin A, Staba R, Crepon B, Wilson CL, Engel J. Cell type-specific firing during ripple oscillations in the hippocampal formation of humans. J Neurosci. 2008;28:6104–6110. doi: 10.1523/JNEUROSCI.0437-08.2008. PubMed DOI PMC

Bagshaw AP, Jacobs J, LeVan P, Dubeau F, Gotman J. Effect of sleep stage on interictal high-frequency oscillations recorded from depth macroelectrodes in patients with focal epilepsy. Epilepsia. 2009;50:617–628. doi: 10.1111/j.1528-1167.2008.01784.x. PubMed DOI PMC

Steriade M, Contreras D, Amzica F. Synchronized sleep oscillations and their paroxysmal developments. Trends Neurosci. 1994;17:199–208. doi: 10.1016/0166-2236(94)90104-X. PubMed DOI

Dinner DS. Effect of sleep on epilepsy. J Clin Neurophysiol. 2002;19:504–513. doi: 10.1097/00004691-200212000-00003. PubMed DOI

De Guzman PH, Nazer F, Dickson CT. Short-duration epileptic discharges show a distinct phase preference during ongoing hippocampal slow oscillations. J Neurophysiol. 2010;104:2194–2202. doi: 10.1152/jn.00418.2010. PubMed DOI

Polich J. Updating p300: an integrative theory of P3a and P3b. Clin Neurophysiol. 2007;118:2128–2148. doi: 10.1016/j.clinph.2007.04.019. PubMed DOI PMC

Girardeau G, Benchenane K, Wiener SI, Buzsaki G, Zugaro MB. Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci. 2009;12:1222–1223. doi: 10.1038/nn.2384. PubMed DOI

Ego-Stengel V, Wilson MA. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus. 2010;20:1–10. PubMed PMC

Nokia MS, Mikkonen JE, Penttonen M, Wikgren J. Disrupting neural activity related to awake-state sharp wave-ripple complexes prevents hippocampal learning. Front Behav Neurosci. 2012;6:84. doi: 10.3389/fnbeh.2012.00084. PubMed DOI PMC

Miller KJ, Zanos S, Fetz EE, den Nijs M, Ojemann JG. Decoupling the cortical power spectrum reveals real-time representation of individual finger movements in humans. J Neurosci. 2009;29:3132–3137. doi: 10.1523/JNEUROSCI.5506-08.2009. PubMed DOI PMC

Manning JR, Jacobs J, Fried I, Kahana MJ. Broadband shifts in local field potential power spectra are correlated with single-neuron spiking in humans. J Neurosci. 2009;29:13613–13620. doi: 10.1523/JNEUROSCI.2041-09.2009. PubMed DOI PMC

Kucewicz MT, Cimbalnik J, Matsumoto JY, Brinkmann BH, Bower MR, Vasoli V, et al. High frequency oscillations are associated with cognitive processing in human recognition memory. Brain. 2014;137(Pt 8):2231–2244. doi: 10.1093/brain/awu149. PubMed DOI PMC

Brazdil M, Dobsik M, Mikl M, Hlustik P, Daniel P, Pazourkova M, et al. Combined event-related fMRI and intracerebral ERP study of an auditory oddball task. Neuroimage. 2005;26:285–293. doi: 10.1016/j.neuroimage.2005.01.051. PubMed DOI

Matsumoto A, Brinkmann BH, Stead SM, Matsumoto J, Kucewicz MT, Marsh WR, et al. Pathological and physiological high-frequency oscillations in focal human epilepsy. J Neurophysiol. 2013;110:1958–1964. doi: 10.1152/jn.00341.2013. PubMed DOI PMC

Jefferys JGR, de la Prida L, Wendling F, Bragin A, Avoli M, Timofeev I, et al. Mechanisms of physiological and epileptic HFO generation. Prog Neurobiol. 2012;98:250–264. doi: 10.1016/j.pneurobio.2012.02.005. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace