nach oben

Journal of Neurology

Erschienen in:

01.12.2009 | Original Communication

Remote effects of hippocampal damage on default network connectivity in the human brain

verfasst von: Lars Frings, Andreas Schulze-Bonhage, Joachim Spreer, Kathrin Wagner

Erschienen in: Journal of Neurology | Ausgabe 12/2009

Einloggen, um Zugang zu erhalten

Abstract

In the healthy human brain the hippocampus is known to work in concert with a variety of cortical brain regions. It has recently been linked to the default network of the brain, with the precuneus being its core hub. Here we studied the remote effects of damage to the hippocampus on functional connectivity patterns of the precuneus. From 14 epilepsy patients with selective, unilateral hippocampal sclerosis and 8 healthy control subjects, we acquired functional MRI data during performance of an object-location memory task. We assessed functional connectivity of a functionally defined region in the precuneus, which showed the typical properties of the default network: significant task-related deactivation, which was reduced in patients compared to control subjects. In control subjects, a largely symmetrical pattern of functional coherence to the precuneus emerged, including canonical default network areas such as ventral medial prefrontal cortex, inferior parietal cortex, and the hippocampi. Assessment of group differences within the default network areas revealed reduced connectivity to the precuneus in ipsilesional middle temporal gyrus and hippocampus in left hippocampal sclerosis patients compared to controls. Furthermore, left hippocampal sclerosis patients showed lower connectivity than right hippocampal sclerosis patients in left middle temporal gyrus, ventral medial prefrontal cortex, and left amygdala. We report remote effects of unilateral hippocampal damage on functional connectivity between distant brain regions associated with the default network of the human brain. These preliminary results underline the impact of circumscribed pathology on functionally connected brain regions.

Greicius MD, Menon V (2004) Default-mode activity during a passive sensory task: uncoupled from deactivation but impacting activation. J Cogn Neurosci 16:1484–1492CrossRefPubMed

Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541CrossRefPubMed

Horovitz SG, Fukunaga M, de Zwart JA, van Gelderen P, Fulton SC, Balkin TJ et al (2008) Low frequency BOLD fluctuations during resting wakefulness and light sleep: a simultaneous EEG–fMRI study. Hum Brain Mapp 29:671–682CrossRefPubMed

Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711CrossRefPubMed

Eichenbaum H (2000) A cortical-hippocampal system for declarative memory. Nat Rev Neurosci 1:41–50CrossRefPubMed

Babb TL, Brown WJ (1987) Pathological findings in epilepsy. In: Engel J (ed) Surgical treatment of the epilepsies. Raven Press, New York, pp 511–540

Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11–21CrossRefPubMed

Saling MM, Berkovic SF, O’Shea MF, Kalnins RM, Darby DG, Bladin PF (1993) Lateralization of verbal memory and unilateral hippocampal sclerosis: evidence of task-specific effects. J Clin Exp Neuropsychol 60:8–618

Focke NK, Thompson PJ, Duncan JS (2008) Correlation of cognitive functions with voxel-based morphometry in patients with hippocampal sclerosis. Epilepsy Behav 12:472–476CrossRefPubMed

10.

Bonilha L, Alessio A, Rorden C, Baylis G, Damasceno BP, Min LL et al (2007) Extrahippocampal gray matter atrophy and memory impairment in patients with medial temporal lobe epilepsy. Hum Brain Mapp 28:1376–1390CrossRefPubMed

11.

Jokeit H, Seitz RJ, Markowitsch HJ, Neumann N, Witte OW, Ebner A (1997) Prefrontal asymmetric interictal glucose hypometabolism and cognitive impairment in patients with temporal lobe epilepsy. Brain 120:2283–2294CrossRefPubMed

12.

Wagner K, Frings L, Halsband U, Everts R, Buller A, Spreer J et al (2007) Hippocampal functional connectivity reflects verbal episodic memory network integrity. Neuroreport 18:1719–1723CrossRefPubMed

13.

Marques CM, Caboclo LO, da Silva TI, Noffs MH, Carrete HJ, Lin K et al (2007) Cognitive decline in temporal lobe epilepsy due to unilateral hippocampal sclerosis. Epilepsy Behav 10:477–485CrossRefPubMed

14.

Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain’s default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 1124:1–38CrossRefPubMed

15.

Fransson P, Marrelec G (2008) The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: evidence from a partial correlation network analysis. Neuroimage 42:1178–1184CrossRefPubMed

16.

Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMed

17.

Van Paesschen W (2004) Qualitative and quantitative imaging of the hippocampus in mesial temporal lobe epilepsy with hippocampal sclerosis. Neuroimaging Clin N Am 14:373–400 viiCrossRefPubMed

18.

Helmstaedter C, Durwen HF (1990) The Verbal Learning and Retention Test. A useful and differentiated tool in evaluating verbal memory performance. Schweiz Arch Neurol Psychiatr 141:21–30PubMed

19.

Lamberti G, Weidlich S (1999) DCS—a visual learning and memory test for neuropsychological assessment. Hogrefe and Huber, Seattle

20.

Frings L, Wagner K, Halsband U, Schwarzwald R, Zentner J, Schulze-Bonhage A (2008) Lateralization of hippocampal activation differs between left and right temporal lobe epilepsy patients and correlates with postsurgical verbal learning decrement. Epilepsy Res 78:161–170CrossRefPubMed

21.

Friston KJ, Holmes A, Worsley K, Poline J, Frith C, Frackowiak R (1995) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2:189–210CrossRef

22.

Kahn I, Andrews-Hanna JR, Vincent JL, Snyder AZ, Buckner RL (2008) Distinct cortical anatomy linked to subregions of the medial temporal lobe revealed by intrinsic functional connectivity. J Neurophysiol 100:129–139CrossRefPubMed

23.

Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci USA 98:676–682CrossRefPubMed

24.

Wagner AD, Shannon BJ, Kahn I, Buckner RL (2005) Parietal lobe contributions to episodic memory retrieval. Trends Cogn Sci 9:445–453CrossRefPubMed

25.

Schacter DL, Addis DR, Buckner RL (2008) Episodic simulation of future events: concepts, data, and applications. Ann N Y Acad Sci 1124:39–60CrossRefPubMed

26.

Hassabis D, Kumaran D, Vann SD, Maguire EA (2007) Patients with hippocampal amnesia cannot imagine new experiences. Proc Natl Acad Sci USA 104:1726–1731CrossRefPubMed

27.

Andreasen NC, O’Leary DS, Cizadlo T, Arndt S, Rezai K, Watkins GL et al (1995) Remembering the past: two facets of episodic memory explored with positron emission tomography. Am J Psychiatry 152:1576–1585PubMed

28.

Gusnard DA, Akbudak E, Shulman GL, Raichle ME (2001) Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proc Natl Acad Sci USA 98:4259–4264CrossRefPubMed

29.

Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583CrossRefPubMed

30.

Rombouts SA, Barkhof F, Goekoop R, Stam CJ, Scheltens P (2005) Altered resting state networks in mild cognitive impairment and mild Alzheimer’s disease: an fMRI study. Hum Brain Mapp 26:231–239CrossRefPubMed

31.

Dickerson BC, Sperling RA (2008) Functional abnormalities of the medial temporal lobe memory system in mild cognitive impairment and Alzheimer’s disease: insights from functional MRI studies. Neuropsychologia 46:1624–1635CrossRefPubMed

32.

Baliki MN, Geha PY, Apkarian AV, Chialvo DR (2008) Beyond feeling: chronic pain hurts the brain, disrupting the default-mode network dynamics. J Neurosci 28:1398–1403CrossRefPubMed

33.

Pantelis C, Velakoulis D, McGorry PD, Wood SJ, Suckling J, Phillips LJ et al (2003) Neuroanatomical abnormalities before and after onset of psychosis: a cross-sectional and longitudinal MRI comparison. Lancet 361:281–288CrossRefPubMed

34.

Greicius M (2008) Resting-state functional connectivity in neuropsychiatric disorders. Curr Opin Neurol 24:424–430CrossRef

35.

Addis DR, Moscovitch M, McAndrews MP (2007) Consequences of hippocampal damage across the autobiographical memory network in left temporal lobe epilepsy. Brain 130:2327–2342CrossRefPubMed

36.

Gleissner U, Helmstaedter C, Schramm J, Elger CE (2004) Memory outcome after selective amygdalohippocampectomy in patients with temporal lobe epilepsy: one-year follow-up. Epilepsia 45:960–962CrossRefPubMed

37.

Bonilha L, Rorden C, Halford JJ, Eckert M, Appenzeller S, Cendes F et al (2007) Asymmetrical extra-hippocampal grey matter loss related to hippocampal atrophy in patients with medial temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 78:286–294CrossRefPubMed

38.

Carrete HJ, Abdala N, Lin K, Caboclo LO, Centeno RS, Sakamoto AC et al (2007) Temporal pole signal abnormality on MR imaging in temporal lobe epilepsy with hippocampal sclerosis: a fluid-attenuated inversion-recovery study. Arq Neuropsiquiatr 65:553–560PubMed

39.

He BJ, Snyder AZ, Vincent JL, Epstein A, Shulman GL, Corbetta M (2007) Breakdown of functional connectivity in frontoparietal networks underlies behavioral deficits in spatial neglect. Neuron 53:905–918CrossRefPubMed

40.

Ranganath C, Heller A, Cohen MX, Brozinsky CJ, Rissman J (2005) Functional connectivity with the hippocampus during successful memory formation. Hippocampus 15:997–1005CrossRefPubMed

41.

Van Paesschen W, Dupont P, Van Driel G, Van Billoen H, Maes A (2003) SPECT perfusion changes during complex partial seizures in patients with hippocampal sclerosis. Brain 126:1103–1111CrossRefPubMed

42.

Gotman J, Grova C, Bagshaw A, Kobayashi E, Aghakhani Y, Dubeau F (2005) Generalized epileptic discharges show thalamocortical activation and suspension of the default state of the brain. Proc Natl Acad Sci USA 102:15236–15240CrossRefPubMed

43.

Laufs H, Lengler U, Hamandi K, Kleinschmidt A, Krakow K (2006) Linking generalized spike-and-wave discharges and resting state brain activity by using EEG/fMRI in a patient with absence seizures. Epilepsia 47:444–448CrossRefPubMed

44.

Laufs H, Hamandi K, Salek-Haddadi A, Kleinschmidt AK, Duncan JS, Lemieux L (2007) Temporal lobe interictal epileptic discharges affect cerebral activity in “default mode” brain regions. Hum Brain Mapp 28:1023–1032CrossRefPubMed

45.

Jokeit H, Okujava M, Woermann FG (2001) Carbamazepine reduces memory induced activation of mesial temporal lobe structures: a pharmacological fMRI-study. BMC Neurol 1:6CrossRefPubMed

Titel: Remote effects of hippocampal damage on default network connectivity in the human brain
verfasst von: Lars Frings
Andreas Schulze-Bonhage
Joachim Spreer
Kathrin Wagner
Publikationsdatum: 01.12.2009
Verlag: D. Steinkopff-Verlag
Erschienen in: Journal of Neurology / Ausgabe 12/2009
Print ISSN: 0340-5354
Elektronische ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-009-5233-0

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

Niedriger diastolischer Blutdruck erhöht Risiko für schwere kardiovaskuläre Komplikationen

25.04.2024 Hypotonie Nachrichten

Wenn unter einer medikamentösen Hochdrucktherapie der diastolische Blutdruck in den Keller geht, steigt das Risiko für schwere kardiovaskuläre Ereignisse: Darauf deutet eine Sekundäranalyse der SPRINT-Studie hin.

Frühe Alzheimertherapie lohnt sich

25.04.2024 AAN-Jahrestagung 2024 Nachrichten

Ist die Tau-Last noch gering, scheint der Vorteil von Lecanemab besonders groß zu sein. Und beginnen Erkrankte verzögert mit der Behandlung, erreichen sie nicht mehr die kognitive Leistung wie bei einem früheren Start. Darauf deuten neue Analysen der Phase-3-Studie Clarity AD.

Viel Bewegung in der Parkinsonforschung

25.04.2024 Parkinson-Krankheit Nachrichten

Neue arznei- und zellbasierte Ansätze, Frühdiagnose mit Bewegungssensoren, Rückenmarkstimulation gegen Gehblockaden – in der Parkinsonforschung tut sich einiges. Auf dem Deutschen Parkinsonkongress ging es auch viel um technische Innovationen.

Demenzkranke durch Antipsychotika vielfach gefährdet

23.04.2024 Demenz Nachrichten

Wenn Demenzkranke aufgrund von Symptomen wie Agitation oder Aggressivität mit Antipsychotika behandelt werden, sind damit offenbar noch mehr Risiken verbunden als bislang angenommen.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 12/2009

C-reactive protein in the very early phase of acute ischemic stroke: association with poor outcome and death

HLA class II alleles in patients with multiple sclerosis in the Biscay province (Basque Country, Spain)

Frequency of progranulin mutations in a German cohort of 79 frontotemporal dementia patients

Postpartum relapsing sensory neuritis responsive to intravenous immunoglobulin

An evaluation of the usefulness of neuroimaging for the diagnosis of Japanese encephalitis