Comparison of PET and fMRI activation patterns during declarative memory processes

Summary

Aim: In this study neuronal correlates of encoding and retrieval in paired association learning were compared using two different neuroimaging methods: positron emission tomography (PET) and functional magnetic resonance imaging (fMRI). Methods: 6 right-handed normal male volunteers took part in the study. Each subject underwent six 0-15-butanol PET scans and an fMRI study comprising four single epochs on a different day. The subjects had to learn and retrieve 12 word pairs which were visually presented (highly imaginable words, not semantically related). Results: Mean recall accuracy was 93% in the PET as well as in the fMRI experiment. During encoding and retrieval we found anterior cingulate cortex activation, and bilateral prefrontal cortex activation in both imaging modalities. Furthermore, we demonstrate the importance of the precuneus in episodic memory. With PET the results demonstrate frontopolar activations whereas fMRI fails to show activations in this area probably due to susceptibility artifacts. In fMRI we found additionally parahippocampal activation and due to the whole-brain coverage cerebellar activation during encoding. The distance between the center-of-mass activations in both modalities was 7.2 ± 6.5 mm. Conclusion: There is a preponderance of commonalities in the activation patterns yielded with fMRI and PET. However, there are also important differences. The decision to choose one or the other neuroimaging modality should among other aspects depend on the study design (single subject vs. group study) and the task of interest.

Zusammenfassung

Ziel: Vergleich der beiden Bildgebungsmethoden Positronen-Emissions-Tomographie (PET) und funktionelle Magnetresonanztomographie (fMRT) bei einer deklarativen Gedächtnisaufgabe. Methoden: 6 Probanden wurden sowohl mit einer GE 4096+-PET-Kamera als auch mit einem Siemens Vision MR-Tomographen während einer deklarativen Gedächtnisaufgabe untersucht. Die Gedächtnisaufgabe bestand darin, 12 Wortpaare hochbildhaften Inhaltes zu lernen und dann zu erinnern (visuelle Präsentation). Ergebnisse: Die Gedächtnisleistung (Anteil der richtigen Assoziationen) der Probanden lag sowohl in der PET-als auch in der fMRT-Studie bei 93% ± 9,3%. Während des Lernvorgangs wurden sowohl in der PET als auch in der fMRT Aktivierungen im anterioren cingulären Kortex, im linken und rechten präfrontalen Kortex und im Präcuneus beobachtet. Nur in der fMRT ließ sich während des Lernvorgangs der parahippocampale Kortex mit darstellen. Während der Abfrage zeigten sich Aktivierungen im linken und rechten Präcuneus, im linken präfrontalen Kortex sowie im anterioren cingulären Kortex. Unterschiede finden sich hier vor allem im Bereich des präfrontalen Kortex, da in der fMRT frontopolare Areale aufgrund von Suszeptibilitätsartefakten nicht darstellbar sind. Die lokalen Maxima der kortikalen Regionen, die in beiden Bildgebungsmodalitäten darstellbar sind, lagen im Mittel 7,2 ± 6,5 mm auseinander. Schlussfolgerung: Die Gemeinsamkeiten in den Aktivierungsmustern in der PET und der fMRT überwiegen. Die Wahl der Bildgebungsmodalität für eine Aktivierungsstudie sollte u.a. abhängig vom Design (Einzelsubjekt vs. Gruppenstudie) und untersuchter kortikaler bzw. subkortikaler Struktur (Suszeptibilität, Signalauflösung) getroffen werden.

Keywords

PET - fMRI - declarative memory - paired word associations

Schlüsselwörter

Aktivierungsstudie - PET - fMRT - deklaratives Gedächtnis - gepaarte Wortassoziationen

• Literatur

• 1 Bandettini PA, Wong EC, Hinks RS, Tikofsky RS, Hyde JS. Time course EPI of human brain function during task activation. Magn Reson Med 1992; 25: 390-7.
• 2 Belliveau JW, Kennedy Jr DN, McKinstry RC, Buchbinder BR, Weisskoff RM, Cohen MS, Vevea JM, Brady TJ, Rosen BR. Functional mapping of the human visual cortex by magnetic resonance imaging. Science 1991; 254: 716-9.
• 3 Berridge MS, Adler LP, Nelson AD, Cassidy EH, Muzic RF, Bednarczyk EM, Miraldi F. Measurement of human cerebral blood flow with [150]butanol and positron emission tomography. J Cereb Blood Flow Metab 1991; 11: 707-15.
• 4 Binder JR, Rao SM, Hammeke TA, Frost JA, Bandettini PA, Hyde JS. Effects of stimulus rate on signal response during functional magnetic resonance imaging of auditory cortex. Brain Res Cogn Brain Res 1994; 2: 31-8.
• 5 Clark VP, Keil K, Maisog JM, Courtney S, Ungerleider LG, Haxby JV. Functional magnetic resonance imaging of human visual cortex during face matching: a comparison with positron emission tomography. Neuroimage 1996; 4: 1-15.
• 6 Coull JT, Nobre AC. Where and when to pay attention: the neural systems for directing attention to spatial locations and to time intervals as revealed by both PET and fMRI. J Neurosci 1998; 18: 7426-35.
• 7 Dettmers C, Connelly A, Stephan KM, Turner R, Friston KJ, Frackowiak RS, Gadian DG. Quantitative comparison of functional magnetic resonance imaging with positron emission tomography using a force-related paradigm. Neuroimage 1996; 4: 201-9.
• 8 Fletcher PC, Dolan RJ, Frith CD. The functional anatomy of memory. Experientia 1995a 51: 1197-207.
• 9 Fox PT, Raichle ME. Stimulus rate dependence of regional cerebral blood flow in human striate cortex, demonstrated by positron emission tomography. J Neurophysiol 1984; 51: 1109-20.
• 10 Fox PT, Raichle ME, Mintun MA, Dence C. Nonoxidative glucose consumption during focal physiologic neural activity. Science 1988; 241: 462-4.
• 11 Frackowiak RS, Lenzi GL, Jones T, Heather JD. Quantitative measurement of regional cerebral blood flow and oxygen metabolism in man using 150 and positron emission tomography: theory, procedure, and normal values. J Cornput Assist Tomogr 1980; 4: 727-36.
• 12 Frostig RD, Lieke EE, Ts’o DY, Grinvald A. Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. Proc Natl Acad Sei USA 1990; 87: 6082-6.
• 13 Fuster JM. (ed). Memory in the cerebral cortex. Cambridge, MA: MIT press; 1995
• 14 Halsband U, Krause BJ, Schmidt D, Herzog H, Tellmann L, Muller-Gartner HW. Encoding and retrieval in declarative learning: a positron emission tomography study. Behav Brain Res 1998; 97: 69-78.
• 15 Herscovitch P, Raichle ME, Kilbourn MR, Welch MJ. Positron emission tomographic measurement of cerebral blood flow and permeability-surface area product of water using [150]water and [llC]butanol. J Cereb Blood Flow Metab 1987; 7: 527-42.
• 16 Herzog H, Seitz RJ, Tellmann L. et al. Quantitation of regional cerebral blood flow with 0-15-butanol and positron emission tomography in humans. J Cereb Blood Flow Metab 1996; 16: 645-9.
• 17 Jensen KB, Hoedt-Rasmussen K, Sveinsdottir E, Lassen NA. Regional cerebral blood flow determined by inhalation of xenon-133. Summary of a methodological study. Acta Neurol Scand Suppl 1965; 13: 309-10.
• 18 Krause BJ, Schmidt D, Mottaghy FM, Halsband U, Teilmann L, Herzog H, Muller-Gartner HW. [O-15-butanol Pet activation study on the cerebral representation of declarative memory], [Article in German]. Nuklearmedizin 1998; 37: 257-61.
• 19 Krause BJ, Schmidt D, Mottaghy FM, Taylor J, Halsband U, Herzog H, Tellmann L, Muller-Gartner HW. Episodic retrieval activates the precuneus irrespective of the imagery content of word pair associates. A PET study. Brain 1999; 122: 255-63.
• 20 Kwong KK, Belliveau JW, Chesler DA, Goldberg IE, Weisskoff RM, Poncelet BP, Kennedy DN, Hoppel BE, Cohen MS, Turner R, Cheng HM, Brady TJ, Rosen BR. Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc Natl Acad Sei USA 1992; 89: 5675-9.
• 21 Lou HC, Edvinsson L, MacKenzie ET. The concept of coupling blood flow to brain function: revision required?. Ann Neurol 1987; 22: 289-97.
• 22 Malonek D, Grinvald A. Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: implications for functional brain mapping. Science 1996; 272: 551-4.
• 23 Menon RS, Ogawa S, Hu X, Strupp JP, Anderson P, Ugurbil K. BOLD based functional MRI at 4 Tesla includes a capillary bed contribution: echo-planar imaging correlates with previous optical imaging using intrinsic signals. Magn Reson Med 1995; 33: 453-9.
• 24 Mottaghy FM, Shah NJ, Krause BJ, Schmidt D, Halsband U, Jancke L, Muller-Gartner HW. Neuronal correlates of encoding and retrieval in episodic memory during a paired-word association learning task: a functional magnetic resonance imaging study. Exp Brain Res 1999; 128: 332-42.
• 25 Ojemann JG, Akbudak E, Snyder AZ, McKinstry RC, Raichle ME, Conturo TE. Anatomic localization and quantitative analysis of gradient refocused echo-planar fMRI susceptibility artifacts. Neuroimage 1997; 6: 156-67.
• 26 Ojemann JG, Buckner RL, Akbudak E, Snyder AZ, Ollinger JM, McKinstry RC, Rosen BR, Petersen SE, Raichle ME, Conturo TE. Functional MRI studies of word-stem completion: reliability across laboratories and comparison to blood flow imaging with PET. Hum Brain Mapp 1998; 6: 203-15.
• 27 Paulesu E, Connelly A, Frith CD, Friston KJ, Heather J, Myers R, Gadian DG, Frackowiak RS. Functional MR imaging correlations with positron emission tomography. Initial experience using a cognitive activation paradigm on verbal working memory. Neuroimaging Clin N Am 1995; 5: 207-25.
• 28 Posner MI, Petersen SE. The attention system of the human brain. Annu Rev Neurosci 1990; 13: 25-42.
• 29 Quarles RP, Mintun MA, Larson KB, Markham J, MacLeod AM, Raichle ME. Measurement of regional cerebral blood flow with positron emission tomography: a comparison of [150]-water to [llC]butanol with distributed-parameter and compartmental models. J Cereb Blood Flow Metab 1993; 13: 733-47.
• 30 Raichle ME, Martin WR, Herscovitch P, Mintun MA, Markham J. Brain blood flow measured with intravenous H2(15)0. II. Implementation and validation. J Nucl Med 1983; 24: 790-8.
• 31 Rees G, Howseman A, Josephs O, Frith CD, Friston KJ, Frackowiak RS, Turner R. Characterizing the relationship between BOLD contrast and regional cerebral blood flow measurements by varying the stimulus presentation rate. Neuroimage 1997; 6: 270-8.
• 32 Roy CS, Sherrington CS. On the regulation of the blood supply of the brain. J Physiol 1890; 4: 85-108.
• 33 Sadato N, Yonekura Y, Yamada H, Nakamura S, Waki A, Ishii Y. Activation patterns of covert word generation detected by fMRI: comparison with 3D PET. J Comput Assist Tomogr 1998; 22: 945-52.
• 34 Schmahmann JD, Sherman JC. Cerebellar cognitive affective syndrome. Int Rev Neurobiol 1997; 41: 433-40.
• 35 Schmidt D, Weckesser M, Krause BJ, Grunwald T, Elger CE, Müller-Gärtner HW. Veränderungen des regionalen zerebralen Blutflusses in Patienten mit linksseitiger Temporallappenepilepsie und Gesunden während deklarativer Gedächtnisprozesse. Nuklearmedizin 1999; 38: 60.
• 36 Small SL, Noll DC, Perfetti CA, Hlustik P, Wellington R, Schneider W. Localizing the lexicon for reading aloud:replication of a PET study using fMRI. Neuroreport 1996; 7: 961-5.
• 37 Talairach J, Tounoux P. (eds). Co-planar stereotactic atlas of the human brain: 3-dimensional proportional system: An approach to cerebral imaging. Stuttgart: Thieme; 1988
• 38 The Wellcome Department of Cognitive Neurology, London. http://www.fil.ion.bpmf.ac.uk
• 39 Votaw JR, Faber TL, Popp CA, Henry TR, Trudeau JD, Woodard JL, Mao H, Hoffman JM, Song AW. A confrontational naming task produces congruent increases and decreases in PET and fMRI. Neuroimage 1999; 10: 347-56.
• 40 Wagner AD, Koutstaal W, Schacter DL. When encoding yields remembering: insights from event-related neuroimaging. Philos Trans R Soc Lond B Biol Sei 1999; 354: 1307-24.
• 41 Wise R, Chollet F, Hadar U, Friston K, Hoffner E, Frackowiak RJS. Distribution of cortical neural networks involved in word comprehension and word retrieval. Brain 1991; 114: 1803-17.
• 42 Xiong J, Rao S, Gao JH, Woldorff M, Fox PT. Evaluation of hemispheric dominance for languageusing functional MRI: a comparison with positron emission tomography. Hum Brain Mapp 1998; 6: 42-58.