Correlations and dissociations between BOLD signal and P300 amplitude in an auditory oddball task: a parametric approach to combining fMRI and ERP

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Abstract

A parametric method is proposed to examine the relationship between neuronal activity, measured with event related potentials (ERPs), and the hemodynamic response, observed with functional magnetic resonance imaging (fMRI), during an auditory oddball paradigm. After verifying that the amplitude of the evoked response P300 increases as the probability of oddball target presentation decreases, we explored the corresponding effect of target frequency on the fMRI signal. We predicted and confirmed that some regions that showed activation changes following each oddball are affected by the rate of presentation of the oddballs, or the probability of an oddball target. We postulated that those regions that increased activation with decreasing probability might be responsible for the corresponding changes in the P300 amplitude.

fMRI regions that correlated with the amplitude of the P300 wave were supramarginal gyri, thalamus, insula and right medial frontal gyrus, and are presumably sources of the P300 wave. Other regions, such as anterior and posterior cingulate cortex, were activated during the oddball paradigm but their fMRI signal changes were not correlated with the P300 amplitudes. This study thus shows how combining fMRI and ERP in a parametric design identifies task-relevant sources of activity and allows separation of regions that have different response properties.

Introduction

The oddball paradigm, in which a distinct -target- stimulus is presented infrequently and at random intervals within a series of frequent -regular- stimuli, has been extensively investigated since it was described by Sutton in 1965. The brain activity elicited can be detected with electrical recordings from the scalp. The P300 is the characteristic endogenous positive wave, arising between 260 and 500 ms after the onset of each rare stimulus, that is more prominent over the centro-parietal region of the scalp [1]. Changes in the latency of the P300 have been associated, among other factors, with aging, psychiatric disorders, task difficulty and memory performance [2], [3]. Changes in the magnitude of the P300 have been related to the experimental conditions as well as to specific changes in information processing by the brain due to experimental manipulation or changes in attention level. In particular, it has been shown that sequence [4] and probability of occurrence of the target stimuli [5], [6], [7] have an effect on the amplitude of the P300. The amplitude of the P300 increases as the probability of occurrence of the oddball decreases. Recently, it has been argued that the differences are not due to probability but rather to target-to-target interval [8].

Despite the good temporal characterization of the electrical response to the oddball paradigm, it is not clear where this potential is generated in the brain. Electrocortical recordings [9], [10] and lesion studies [11] have suggested that temporal, parietal and frontal regions, as well as limbic structures, are involved in the P300 generation.

In recent years, fMRI has developed as a powerful tool for localizing brain activation. Studies conducted by our group and others [12], [13], [14], [15], [16] agree upon the involvement of parietal areas, particularly supramarginal gyrus, in the response to the oddball task. Depending on modality (i.e., visual or auditory stimuli) or response type (button press or silent counting) some other regions, including frontal and temporal areas and cingulate cortex, have also been reported as activated by the oddball paradigm.

ERP and fMRI data have complementary abilities to describe brain function, with different temporal and spatial resolutions, and there is considerable interest in better understanding how neuronal electrical activity may be related to the hemodynamic and metabolic changes seen in imaging. Thus, the purpose of this work was to explore the correlations and dissociations between the amplitude of the P300 wave and changes in Blood Oxygenation Level Dependent (BOLD) fMRI signals. During these experiments, we changed the frequency of occurrence of the oddball stimuli in four steps. We kept constant the intensity of the stimuli and the inter-stimulus interval throughout the experiment and explored which brain regions were affected by the experimental manipulation. The parallel changes in ERP and fMRI signal in such a parametric design provides a novel method for connecting these two different modalities.

Section snippets

Subjects

Seven healthy subjects (average age = 27 years, range = 21–37 years, 2 females) participated in this study, having previously provided their informed consent in accordance with a protocol reviewed and approved by the Human Investigation Committee of Yale University School of Medicine.

Stimulus presentation

Computer-generated auditory stimuli were presented to the subjects every 1.5 s using the shareware software: “PsyScope” (Department of Psychology, Carnegie Mellon University) and “SoundSculptorII.” The frequent

ERP

All subjects showed a P300 response to the oddball stimulus. The activity was more prominent over the centro-parietal area (Fig. 3a).

There was a significant effect of probability of oddball (F(3,18) = 3.936, p < 0.046 Greenhouse-Geisser corrected for sphericity) and also a significant linear contrast effect (within subject, TTI level: F(1,6) = 8.052, p < 0.030; electrode: F(1,6) = 12.009, p < 0.013). The TTI effect was more significant at electrode Fz (F(3,18) = 4.452 p < 0.030

Discussion

The results obtained for the electrical recording agree with those of Duncan-Johnson [7] and others. As expected, the P300 was more prominent in the centro-parietal electrodes, being maximum at Pz, and it increased in amplitude as the oddball became less frequent. The electrode affected the most by the experimental manipulation was Fz. The observed effect was small. Picton reviewed the TTI effect as reported in the literature [2] and showed a small increase in amplitude as the TTI increased for

Acknowledgements

We wish to acknowledge Dr. M. Torello, Capital University, Columbus, OH, for useful discussions in the early stages of this work and T. Hickey and H. Serofin, Yale University, for their help in the fMRI experiments.

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