SummaryImaging human brain function with techniques such as magnetoencephalography1 (MEG) typically requires a subject to perform tasks whilst their head remains still within a restrictive scanner. This artificial environment makes the technique inaccessible to many people, and limits the experimental questions that can be addressed. For example, it has been difficult to apply neuroimaging to investigation of the neural substrates of cognitive development in babies and children, or in adult studies that require unconstrained head movement (e.g. spatial navigation). Here, we develop a new type of MEG system that can be worn like a helmet, allowing free and natural movement during scanning. This is possible due to the integration of new quantum sensors2,3 that do not rely on superconducting technology, with a novel system for nulling background magnetic fields. We demonstrate human electrophysiological measurement at millisecond resolution whilst subjects make natural movements, including head nodding, stretching, drinking and playing a ball game. Results compare well to the current state-of-the-art, even when subjects make large head movements. The system opens up new possibilities for scanning any subject or patient group, with myriad applications such as characterisation of the neurodevelopmental connectome, imaging subjects moving naturally in a virtual environment, and understanding the pathophysiology of movement disorders.

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Unambiguous interpretation of changes in the BOLD signal is challenging because of the complex neurovascular coupling that translates changes in neuronal activity into the subsequent haemodynamic response. In particular, the neurophysiological origin of the negative BOLD response (NBR) remains incompletely understood. Here, we simultaneously recorded BOLD, EEG and cerebral blood flow (CBF) responses to 10 s blocks of unilateral median nerve stimulation (MNS) in order to interrogate the NBR. Both negative BOLD and negative CBF responses to MNS were observed in the same region of the ipsilateral primary sensorimotor cortex (S1/M1) and calculations showed that MNS induced a decrease in the cerebral metabolic rate of oxygen consumption (CMRO2) in this NBR region. The ∆CMRO2/∆CBF coupling ratio (n) was found to be significantly larger in this ipsilateral S1/M1 region (n=0.91±0.04, M=10.45%) than in the contralateral S1/M1 (n=0.65±0.03, M=10.45%) region that exhibited a positive BOLD response (PBR) and positive CBF response, and a consequent increase in CMRO2 during MNS. The fMRI response amplitude in ipsilateral S1/M1 was negatively correlated with both the power of the 8-13 Hz EEG mu oscillation and somatosensory evoked potential amplitude. Blocks in which the largest magnitude of negative BOLD and CBF responses occurred therefore showed greatest mu power, an electrophysiological index of cortical inhibition, and largest somatosensory evoked potentials. Taken together, our results suggest that a neuronal mechanism underlies the NBR, but that the NBR may originate from a different neurovascular coupling mechanism to the PBR, suggesting that caution should be taken in assuming the NBR simply represents the neurophysiological inverse of the PBR.

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Massed synchronised neuronal firing is detrimental to information processing. When networks of task-irrelevant neurons fire in unison, they mask the signal generated by task-critical neurons. On a macroscopic level, such synchronisation can contribute to alpha/beta (8–30 Hz) oscillations. Reducing the amplitude of these oscillations, therefore, may enhance information processing. Here, we test this hypothesis. Twenty-one participants completed an associative memory task while undergoing simultaneous EEG-fMRI recordings. Using representational similarity analysis, we quantified the amount of stimulus-specific information represented within the BOLD signal on every trial. When correlating this metric with concurrently-recorded alpha/beta power, we found a significant negative correlation which indicated that as post-stimulus alpha/beta power decreased, stimulus-specific information increased. Critically, we found this effect in three unique tasks: visual perception, auditory perception, and visual memory retrieval, indicating that this phenomenon transcends both stimulus modality and cognitive task. These results indicate that alpha/beta power decreases parametrically track the fidelity of both externally-presented and internally-generated stimulus-specific information represented within the cortex.

Large artefacts compromise EEG data quality during simultaneous fMRI. These artefact voltages pose heavy demands on the bandwidth and dynamic range of EEG amplifiers and mean that even small fractional variations in the artefact voltages give rise to significant residual artefacts after average artefact subtraction. Any intrinsic reduction in the magnitude of the artefacts would be highly advantageous, allowing data with a higher bandwidth to be acquired without amplifier saturation, as well as reducing the residual artefacts that can easily swamp signals from brain activity measured using current methods. Since these problems currently limit the utility of simultaneous EEG-fMRI, new approaches for reducing the magnitude and variability of the artefacts are required. One such approach is the use of an EEG cap that incorporates electrodes embedded in a reference layer that has similar conductivity to tissue and is electrically isolated from the scalp. With this arrangement, the artefact voltages produced on the reference layer leads by time-varying field gradients, cardiac pulsation and subject movement are similar to those induced in the scalp leads, but neuronal signals are not detected in the reference layer. Taking the difference of the voltages in the reference and scalp channels will therefore reduce the artefacts, without affecting sensitivity to neuronal signals. Here, we test this approach by using a simple experimental realisation of the reference layer to investigate the artefacts induced on the leads attached to the reference layer and scalp and to evaluate the degree of artefact attenuation that can be achieved via reference layer artefact subtraction (RLAS). Through a series of experiments on phantoms and human subjects, we show that RLAS significantly reduces the gradient (GA), pulse (PA) and motion (MA) artefacts, while allowing accurate recording of neuronal signals. The results indicate that RLAS generally outperforms AAS when motion is present in the removal of the GA and PA, while the combination of AAS and RLAS always produces higher artefact attenuation than AAS. Additionally, we demonstrate that RLAS greatly attenuates the unpredictable and highly variable MAs that are very hard to remove using post-processing methods.

EEG recordings made during concurrent fMRI are confounded by the pulse artefact (PA), which although smaller than the gradient artefact is often more problematic because of its variability over multiple cardiac cycles. A better understanding of the PA is needed in order to generate improved methods for reducing its effect in EEG–fMRI experiments. Here we performed a study aimed at identifying the relative contributions of three putative sources of the PA (cardiac-pulse-driven head rotation, the Hall effect due to pulsatile blood flow and pulse-driven expansion of the scalp) to its amplitude and variability. EEG recordings were made from 6 subjects lying in a 3 T scanner. Accelerometers were fixed on the forehead and temple to monitor head motion. A bite-bar and vacuum cushion were used to restrain the head, thus greatly attenuating the contribution of cardiac-driven head rotation to the PA, while an insulating layer placed between the head and the EEG electrodes was used to eliminate the Hall voltage contribution. Using the root mean square (RMS) amplitude of the PA averaged over leads and time as a measure of the PA amplitude, we found that head restraint and insulating layer reduced the PA by 61% and 42%, respectively, when compared with the PA induced with the subject relaxed, indicating that cardiac-pulse-driven head rotation is the dominant source of the PA. With both the insulating layer and head restraint in place, the PA was reduced in RMS amplitude by 78% compared with the relaxed condition, the remaining PA contribution resulting from scalp expansion or residual head motion. The variance of the PA across cardiac cycles was more strongly reduced by the insulating layer than the head restraint, indicating that the flow-induced Hall voltage makes a larger contribution than pulse-driven head rotation to the variability of the PA.

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