Interhemispheric connectivity during spontaneous switches in visual perceptual coherence as revealed by fMRI at multiple temporal resolutions

doi:10.21203/rs.3.rs-4335511/v1

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Interhemispheric connectivity during spontaneous switches in visual perceptual coherence as revealed by fMRI at multiple temporal resolutions

https://doi.org/10.21203/rs.3.rs-4335511/v1

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Functional magnetic resonance imaging (fMRI) allows to observe neural activity in real-time but tracking the neural correlates of perceptual decision as a function of interhemispheric connectivity has remained difficult. Recent advances in image acquisition, namely with the surfacing of multiband sequences, have led us to investigate this mechanism using higher temporal resolution approaches. We were able to better capture the hemodynamic responses to rapid changes in neural activity concomitantly with a task requiring either perceptual interhemispheric segregation or integration, shortening the gap to other neuroimaging techniques, which is particularly significant when considering the study of dynamic connectivity patterns. Here, we tested the hypothesis whether interhemispheric connectivity in the visual cortex relates to interhemispheric integration, when presented with bistable moving stimuli at four distinct temporal resolutions. Based on this connectivity metric, we could discern perceptual state transitions related to connectivity. First, we found that activation response metrics to visual motion in our target region of interest, the human visual motion complex hMT+, are stable across temporal resolutions. Then, we investigated interhemispheric connectivity between homologous hMT + in response to bistable moving stimuli, for all resolutions, which was critical for replication of perception related interhemispheric synchrony. The established relation between perceptual coherence and increased synchrony across the hemispheres suggests the feasibility of a real-time fMRI neurofeedback based on interhemispheric connectivity. Accordingly, we could infer perceptual states based on this connectivity metric while designing a rule that could even be used to generate feedback. We further showed that higher resolution sequences are beneficial when implementing feedback interfaces based on interhemispheric functional connectivity, both regarding the delay and the accuracy of the feedback itself. Regarding the use of real time fMRI and neurofeedback strategies, higher resolution sequences are likely needed, when relying on connectivity metrics.

Biological sciences/Neuroscience/Cognitive neuroscience/Perception

Biological sciences/Neuroscience/Sensory processing

Biological sciences/Neuroscience/Neural circuit

Visual perception

bistable motion

interhemispheric connectivity

neurofeedback

multiband

fMRI

Functional magnetic resonance imaging (fMRI) has revolutionized our understanding of brain function, and it is now possible to observe neural activity in real-time. One critical aspect in the context of fMRI is its temporal resolution. Unlike other neuroimaging techniques, such as electroencephalography (EEG) or magnetoencephalography (MEG), fMRI has limited temporal resolution, meaning it may not have the sensitivity to capture the hemodynamic responses to rapid changes in neural activity. This aspect becomes particularly significant when considering the study of dynamic connectivity patterns in the human visual system. The perceptual integration of components of motion to generate a global pattern may require communication between different parts of the visual system (Duarte et al., 2017). In the case of bistable perception, the fast changes in interhemispheric connectivity inform us about the binding mechanisms of visual motion features (Sousa et al., 2019). While aiming for a novel intervention that target online perceptual learning mechanisms (Scharnowski et al., 2012), the detection in real-time of functional connectivity changes is key. Hence, in this study, we explore the interhemispheric connectivity in the visual cortex in response to bistable (coherent or incoherent) moving stimuli at different temporal resolutions, to validate and infer perceptual states based on this metric. Online tracking of perception might also help prompt the exploration of a real-time fMRI connectivity based neurofeedback protocol that aims at potentiating cognitive functions in an immersive therapeutic setting. Ultimately, this output of neuroscientific relevance to track interhemispheric integration and perceptual decision would also allows us to generalize the impact of temporal resolution in real time approaches such as neurofeedback paradigms.

Our first goal is to test the hypothesis that the functional dynamics of the human motion complex (hMT+) across hemispheres reflects bistable global motion perception. This region, homologous to the monkey MT region, is a well-known region of the visual cortex that responds to motion in the visual field. Here, we follow previous evidence acquired at 7T that suggested, for the first time, that perceptual long-range integration of bistable motion is linked to the interhemispheric functional connectivity in hMT+ (Sousa et al., 2019). However, that finding remains the single one in the literature suggesting that interhemispheric perceptual integration is mirrored by enhanced functional connectivity across the hemispheres Specifically, the working hypothesis is that interhemispheric functional connectivity hMT+, at the scale of fMRI temporal resolution, reflects perceptual decision (eg. Coherence vs Incoherence). Using a different bistable stimulus (moving plaids, Fig. 1) and a 3T MRI scanner, we aimed to validate these findings at different fMRI temporal resolutions, which depend on the acquisition Repetition Time (TR). Our motivation lies in the ability to detect fast perceptual transitions, in the order of magnitude of the TR, to then explore its neuroscientific potential as well as the possibility of using this information in a neurofeedback setup. We use a moving plaid, which is a bistable visual stimulus that can be seen as two gratings sliding over each other and moving in different directions (incoherent motion) or as a single surface moving coherently – the two gratings are integrated perceptually into a single surface moving coherently in a direction intermediate to the directions of the individual gratings (coherent motion) (Sousa et al., 2018, 2024; Sayal et al., 2020) (Fig. 1)

Multiband echo-planar imaging (MB-EPI) sequences have revolutionized image sampling rates, offering a remarkable increase in temporal resolution. These use advanced pulse sequences and specialized MRI hardware to simultaneously excite and acquire data from multiple slices. By doing so, they can cover a larger volume of the brain or body in a shorter time compared to the sequential acquisition of slices. In clinical applications, these sequences show more detailed BOLD signals with superior temporal resolution and contrast-to-noise ratio, pivotal features for detecting nuanced responses of neuronal populations (Zhang et al., 2024). However, high multiband factors should be used with caution, as discussed in a recent editorial (Wall, 2023).

Given the increasing application of MB sequences for fMRI protocols, a number of studies started to thoroughly evaluate how the BOLD signal was affected by this new acquisition technique (Chen et al., 2015; Todd et al., 2016, 2017; Demetriou et al., 2018; Risk, Kociuba and Rowe, 2018; Jahanian et al., 2019; Bhandari et al., 2020; Renz et al., 2023). These studies compare quality and functional metrics for data acquired with different temporal resolutions (hence multiband factors). For instance, (Chen et al., 2015) results revealed notably higher BOLD information content when employing faster TRs between 300 ms and 600 ms, in contrast to a 2-second TR, indicating that faster TRs can capture more information per unit of time in task-based fMRI studies. Another study (Todd et al. 2016) evaluated BOLD sensitivity and false-positive activations. Based on the results, the authors make recommendations regarding the reconstruction method and the MB factor that allows for a combined low probability of false-positive activations (due to slice leakage) and high quality (fair spatial and temporal resolution) data. Their conservative recommendation limits the MB factor to 2 and in-plane acceleration to 2. In fact, the benefits of these sequences are not always clear. (Demetriou et al. 2018) found that multi-band protocols showed strong benefits for resting-state data analyses and Multi-Voxel Pattern Analyses (MVPA) but not so evident and consistent improvements for task-based paradigms and standard General Linear Model (GLM) approaches, linking these results to variations in temporal signal-to-noise-ratio (SNR) between sequences. (Srirangarajan et al., 2021) provided a cautionary note regarding the study of mesolimbic regions with multiband sequences, as the authors found reductions in temporal SNR that could account for impaired detection of task-related responses in these deeper regions in the brain.

Neurofeedback (NF) experiments based on real-time fMRI have opened the possibility for individuals to self-regulate specific not only brain activation but now also connectivity patterns. This is achieved by interpreting a feedback signal and exploring the appropriate strategies for its modulation. Currently, the impact of several protocol parameters with special attention given to exploring the influence of different self-regulation strategies, feedback interfaces, and data analysis pipelines (Sitaram et al., 2017; Hampson, Ruiz and Ushiba, 2020; Ros et al., 2020; Weber, Ethofer and Ehlis, 2020). As was recently demonstrated (Kadosh and Staunton, 2019), psychological variables such as motivation or mood correlate with the success of neurofeedback.

When feedback is presented in a continuous manner, it requires updating the feedback signal after each fMRI time point. Considering a TR for functional imaging of 2 seconds, we achieve a temporal resolution of 0.5 Hz in the feedback signal. This rather slow update rate of the feedback interface, coupled with the hemodynamic delay between the self-regulation and the feedback, may reduce the efficacy of the protocols. While decreasing the TR does not influence the rate at which neural processes occur nor the response time of the HRF, it may positively impact the immersiveness and the feedback calculation estimates for real-time use. Specifically, this increased temporal resolution could play a role in improving neurofeedback success, as it may contribute to the enhanced reliability of feedback signals based on activation or connectivity measures, providing a more realistic and immersive experience.

In this study, we investigated our working hypothesis of interhemispheric functional connectivity in hMT + during a bistable visual motion task at four temporal resolutions: 2, 1.33, 1, and 0.4 Hz (TR = 0.5, 0.75, 1, and 2.5 seconds, respectively). This led to confirmation that one can link interhemispheric functional connectivity to global coherent perception. Then, we test if the activation metrics of hMT + are replicable across TRs. Finally, by establishing that perception can be read out from connectiviy patterns, we compare and contrast the characteristics of the feedback signal to be provided in a neurofeedback loop based on the activation and connectivity of hMT+. This region has been used in past studies as the target for neurofeedback, aiming for the self-modulation of the activity of this region in real time (Banca et al., 2015; Sousa et al., 2016; Direito et al., 2021). If we aimed to provide feedback on the perceptual switches based on the hMT + inter-hemispheric correlation, we checked how reliable and responsive this feedback would be at different resolutions.

Participants

Fifteen healthy participants were recruited for this experiment (mean age 29.7 ± 8.4 years, 6 females) with normal or corrected-to-normal vision and no history of neurological or psychiatric diseases. All participants were right-handed, as confirmed by a handedness questionnaire adapted from (Oldfield, 1971): mean laterality index of 85.0 ± 9.0. All gave informed written consent before participating in accordance with the declaration of Helsinki, and the study followed the safety guidelines for magnetic resonance imaging research on humans. The work was approved by the Ethics Committee of the Faculty of Medicine of the University of Coimbra.

fMRI data acquisition

Scanning was performed on a 3T Siemens Magnetom Prisma fit, using a 64-channel head/neck coil, at the Institute of Nuclear Sciences Applied to Health (ICNAS), University of Coimbra, Portugal. The scanning session started with the acquisition of one 3D anatomical magnetization-prepared rapid acquisition gradient echo (MPRAGE) pulse sequence (TR = 2530 ms, echo time (TE) = 3.42 ms, flip angle (FA) = 7°, 176 slices, voxel size 1.0 × 1.0 × 1.0 mm³, field of view (FOV) = 256 × 256 mm²).

The functional runs were acquired using a 2D multi-band (MB) gradient-echo (GE) echo-planar imaging (EPI) sequence from the Center for Magnetic Resonance Research, University of Minnesota (Release R016a). We tested four different temporal resolutions: TR = 0.5 s (MB factor = 6, FA = 53º, 42 slices), TR = 0.75 s (MB factor = 4, FA = 63º, 40 slices), TR = 1 s (MB factor = 3, FA = 68º, 42 slices), TR = 2.5 s (MB factor = 1, FA = 85º, 42 slices). The remaining parameters were matched: TE = 30.2 ms, interleaved slices with 0.5 mm gap, voxel size 2.5 × 2.5 × 2.5 mm³, FoV 192 × 192 mm² (Table 1).

Table 1

Main parameters of the four fMRI sequences.
Sequence	1	2	3	4
TR (s)	0.5	0.75	1	2.5
TE (ms)	30.2
MB factor	6	4	3	1
Voxel size (mm)	2.5
Slice gap (mm)	0.5
Number of slices	42	40	42	42
Flip Angle (º)	53	63	68	85
Bandwidth (Hz/px)	2742	2742	2632	1994
Echo Spacing (ms)	0.51	0.49	0.49	0.59
Excite pulse duration (us)	2560	2560	2560	4840
EPI factor	76
GRAPPA	Off	Off	Off	2
LeakBlock	On	On	On	Off

For mapping and correction of image distortions related to magnetic field inhomogeneities, we acquired a pair of spin-echo images with anterior-posterior (AP) and posterior-anterior (PA) phase encoding polarity with matching geometry and echo-spacing to each of the functional scans. These were acquired before the functional runs.

The participants’ physiological signals (respiration and pulse) were recorded during the functional runs using the scanner’s Physiological Measurement Unit (PMU). The respiratory signal was recorded at 50 Hz using a respiratory cushion, and the cardiac cycle was recorded at 200 Hz using a pulse sensor.

Functional tasks

We implemented three functional tasks based on a moving plaid stimulus. These stimuli are created by superimposing two gratings leading to a bistable percept: stimuli can be perceived moving coherently as a single surface (integration) or incoherently as two separate surfaces sliding over each other (segregation) (see supplementary materials and Fig. 1).

The first is a localizer for the region of interest - hMT+. For this purpose, we created three conditions: i. ‘Fixation’ - a fixation cross; ii. ‘Static plaid’ - a stationary plaid; iii. ‘moving plaid’ - a moving plaid, which is inherently a bistable stimulus (coherent versus incoherent, e.g. integration versus segregation). The run lasted for 2.9 min and was composed of nine trials with the sequential presentation of each condition for 6 seconds.

We named the following two tasks as ‘ambiguous’ and ‘unambiguous’ runs. These runs are composed of trials considering three conditions: ‘static’ (static plaid), ‘motion’ (ambiguous or unambiguous moving plaid), and ‘MAE’ (a period during which motion aftereffect is expected). During the ambiguous runs, the ‘motion’ condition showed the participants the moving plaid without any overlaid dots. As such, the stimulus is entirely ambiguous (the percept alternates between coherent and incoherent). Here, the participants were instructed to report the perceived type of motion (coherent or incoherent) using two buttons of a response box. During the unambiguous runs, the plaid is shown with overlaid dots moving either coherently down or incoherently inwards, which disambiguates the perception of the plaid (unambiguously coherent or incoherent). Based on the responses given by the participant in the previous ambiguous run, we manipulated the switches between coherent and incoherent motion in the unambiguous runs to match the previous responses precisely. This matched the time of each percept across both types of runs. The participants received the same instruction - to report the perceived type of motion at all times.

In this work, we considered the localizer and the four unambiguous runs, one for each temporal resolution.

fMRI data preprocessing

The data were organized according to the Brain Imaging Data Structure (BIDS) (Gorgolewski et al., 2016), using BIDSkit (Tyszka, 2023) and dcm2niix (Li et al., 2016). Results included in this manuscript were obtained after data preprocessing performed using fMRIPrep 23.0.2 (Esteban et al., 2023), which is based on Nipype 1.8.6 (Gorgolewski et al., 2011; Esteban et al., 2022). For a detailed description of the fmriPrep pipeline please see supplementary materials. To perform quality checks on the anatomical and functional images and extract metrics for further analysis and sequence comparison we ran mriqc 23.0.1 (Esteban et al., 2017). All subsequent analyses were performed in Python using Nilearn (Abraham et al., 2014).

fMRI data analysis

Regarding the localizer data, hMT + was functionally localized for each subject using a standard GLM analysis. The design matrix included predictors for all experimental conditions (‘fixation’, ‘static plaid', ‘moving plaid’) and confound regressors based on the mean and first derivative of the voxels in the CSF and the six head motion parameters and their derivatives. Temporal high-pass filtering (cut-off = 0.03 Hz) and spatial smoothing (FWHM = 6 mm) were applied. hMT + was manually selected on both hemispheres based on the activation map for the contrast ‘moving plaid > static plaid’ corrected with Bonferroni p = 0.05, cluster threshold k = 50, and confirmed using the hMT + mask of Neurosynth (Yarkoni et al., 2011)). Then, a spherical mask was designed around the center coordinates of each defined ROI (radius = 6 mm).

The first step to analyzing the unambiguous runs was the definition of the coherent and incoherent predictors. To this end, using the perceptual reports acquired via button presses with a temporal resolution of 60 Hz, we calculated the percentage of coherent reports over the total number of reports for each volume. We used this value to label each volume as coherent or incoherent. This information defines which of the two percepts the participant is experiencing at any given time, allowing us to design predictors for coherent and incoherent events (for the GLM analyses) and to have the onsets and offsets of each percept to use for the neurofeedback algorithm.

We estimated the functional activation maps of the unambiguous runs for each TR using a GLM. The design matrix included predictors for all experimental conditions (‘static’, ‘unambiguous motion’, ‘MAE’) and confound regressors based on the mean and first derivative of the voxels in the CSF and the six head motion parameters and their derivatives. Temporal high-pass filtering (cut-off = 0.003 Hz) was applied before extracting ROI activation measures (beta statistic and t-value). Our contrast of interest here was ‘unambiguous motion’ vs. ‘static’.

We then used a different design matrix, replacing the ‘unambiguous motion’ predictor with predictors for coherent and incoherent percepts. As in the previous model, we extract the ROI beta statistic and t-value for the contrasts between coherent/incoherent and static plaid.

For the following analyses, we extract the time course of the ROI and normalize it as a percent signal change to the mean value across time. We estimate the feedback based on this time course as we would in an actual neurofeedback experiment, by displaying the signal variation during the ‘unambiguous motion’ upregulation condition vs. the ‘static’ baseline/downregulation condition.

Next, we use the time courses of the left and right hMT + to estimate Pearson’s correlation over time, a measure of inter-hemispheric functional connectivity. We use a sliding window of 6 seconds for the three lower TRs and of 7.5 seconds for the higher TR (a minimum of 3 data points was considered for obtaining a measurable correlation value). Using the perceptual report information, we center all correlation windows at the transitions between coherent and incoherent percepts and average them across trials and participants. Given the size of the windows, we only considered coherent and incoherent events that lasted at least 7.5 seconds.

To use the functional connectivity information as feedback, we study its characteristics by defining a feedback rule. We defined that successful automatic detection of a perceptual transition meant a 10% minimum increase or decrease in correlation, for coherent and incoherent trials, respectively. We chose this threshold based on (Sousa et al., 2019), which reported an average difference in correlation between percepts of 0.13 ± 0.04. Based on this rule, we extract the transitions’ detection ratio and the time to detection from the first correlation window that includes the volume of transition.

Data and code availability

All the code for the above-mentioned analyses and data (including the activation maps and hMT+ timecourses) can be found at https://github.com/alexsayal/vpmb-tr.

Localizer for hMT+

We defined the left and right hMT + ROIs in the localizer map of each individual, considering the contrast ‘moving’ vs. ‘static’, a voxel-wise correction with Bonferroni’s method (p = 0.05) and cluster-wise with a minimum cluster size of 50 voxels (Fig. 2). The MNI coordinates of the center of the left and right hMT + clusters for each subject are reported in Table S1. The group activation map is shown in Figure S1, and the average MNI coordinates of the center of the left and right clusters are (-42,-72,4) and (48,-66,6), respectively.

GLM statistical values of hMT+

In Fig. 3, we display the outcomes of the GLM analyses performed. In the first column, we plot the beta and t-values of the contrast ‘motion vs. static’. While there is no difference in the beta values between TRs, the t-value of the sequence with the lowest TR is significantly higher than the 2.5 s sequence. This indicates a higher level of certainty in the activation measurement (lower beta error) for the sequence with TR = 0.5 s.

With the coherent and incoherent contrasts, we aimed to test if the measures of activation of rapidly changing events were higher and more reliable for the higher-resolution data. We found a significant difference in the t-value of the coherent contrast, again between the sequences with TR of 0.5 and 2.5 seconds.

Interhemispheric connectivity

In Fig. 4, we display the time courses of interhemispheric correlation of hMT + for all the sequences with different temporal resolutions, centered on the perceptual switches between coherent and incoherent states and vice versa. The results are consistent across TRs - the transition to the coherent percept is linked to an increase in interhemispheric connectivity, while the transition to the incoherent percept is linked to a decrease in connectivity.

BOLD feedback estimation based on the hMT + response

We display the group average hMT + time course for each TR in Fig. 5. This allows the visual comparison between the signals - the difference in temporal resolution is clear while the overall signal variation is similar across TRs. Using these time courses, we simulate a feedback signal to be provided during the motion/upregulation condition. We first normalize the signal to the mean value of the ‘static’, baseline condition, as a percent signal variation. Then, based on a maximum percent signal change of 2.5, we discretize this signal into 10 values, as we would if this information were to be displayed in a visual feedback interface with 10 activation levels. We display both of these signals in Fig. 6 for the four TRs.

While all temporal resolutions provide a valid feedback signal, the variability for the 2.5 s sequence is higher (average SD = 4.97, while for the other sequences, it ranges from 1.39 to 1.60), with the feedback signal achieving values of zero during the upregulation condition. All signals take approximately the same time to reach the peak value of activation (as indicated by the red vertical dashed line).

Feedback characteristics based on interhemispheric functional connectivity

Here, we explored two characteristics of the feedback signal based on interhemispheric hMT + functional connectivity at different resolutions. Based on a rule that could distinguish coherent or incoherent perception, we calculated the percentage of detected switches (Fig. 7) and the time it took to detect such switches (Fig. 8) since the volume of transition for each sequence. The results show statistically significant differences in both metrics between the sequence with TR of 2.5 seconds and the other three sequences.

Here we found that changes in interhemispheric connectivity reliably reflects perceptual integration and decision and becomes more evident with improved temporal resolution as implemented by multiband sequences. We also showed the feasibility of using connectivity based neurofeedback approaches

Improving temporal resolution as a prior to study connectivity

Here we used moving plaid stimuli, that lead to bistable percepts of coherent (reflecting integration) or non coherent (reflecting segregation) motion which lead to different activity levels in visual area hMT+, which may relate to differential profiles of adaptation and inhibition strengths across time for the two percepts (Sousa et al., 2018, 2024; Sayal et al., 2020).

Our first aim was to compare activation metrics across temporal resolutions for each of the conditions, coherent and incoherent motion percepts. The hypothesis was that higher temporal resolution sequences would allow for better activation estimates (i.e. smaller beta error values), which may be critical for subsequent connectivity analysis. Indeed, we found a significant difference between the t-values of the lower and higher temporal resolution sequences for the overall motion and coherent predictors, with higher t-values for the lower TR. This result indicates that higher resolution sequences might benefit rapid-changing events or short blocks, as they provide more points to estimate the GLM and improve the statistical outcomes. These results might, however, be specific to the research question, as (Darányi et al., 2021) found that increasing the temporal resolution of the signal did not universally improve the group-level statistical outcomes, reinforcing the importance of pilot testing and hemodynamic response function estimation for the ROIs being studied.

Functional interhemispheric connectivity reliably reflects perceptual coherence

A recent study emphasized the crucial role of replication by demonstrating that a meta-analytical approach, pooling information across teams, was essential in establishing a significant consensus on activated regions (Rotem Botvinik-Nezer et al., 2020). We previously suggested using roof like stimuli at 7 tesla that interhemispheric functional connectivity reflects perceptual integration (Sousa et al., 2019). Remarkably this hypothesis lacks generalization. Here we confirmed this hypothesis using a different bistable stimulus at a lower field strength and distinct temporal resolutions.

The results of (Sousa et al., 2019) showed opposing variations in hMT + inter-hemispheric correlation when changing either to coherent or incoherent percepts of an ambiguous visual stimulus. The connectivity between the left and right hMT + was shown to be critical in interpreting visual moving stimuli. When studying the “motion quartet”, an ambiguous stimulus that generates horizontal or vertical apparent motion, it was suggested that its perception requires interhemispheric integration, although functional connectivity was not studied (Genç et al., 2011). The authors were able to predict the perception based on structural connectivity data of callosal segments linking both hMT + regions. Howver these authors did not present functional connectivity data. Nevertheles, when the connectivity is manipulated using transcranial magnetic stimulation, the sensitivity to one of the possible percepts increases (Chiappini et al., 2022).

When we analyze the volumes around the transition between coherent and incoherent perceptual states, as reported by the participants, we found a decrease in inter-hemispheric correlation after switching to the incoherent percept and an increase after switching to the coherent percept (Fig. 4), which is consistent with the findings of (Sousa et al., 2019) (see Fig. 4 of that study). One should note that this pioneering study uses a different ambiguous stimulus and a scanner with a higher static magnetic field (7T), but reaches consistent conclusions regarding this visual region activation when processing ambiguous moving stimuli. Moreover, in this study, the findings are replicated for all TRs.

Functional connectivity as feedback of perceptual transitions

We estimate the impact of temporal resolution on a BOLD-based feedback signal in Fig. 6. An intriguing finding is that, for the sequence with the lowest resolution, the variability of the feedback signal is much higher. The standard deviation indicates that the feedback signal is less consistent across participants and that the mean even reaches zero at some points along the ‘upregulation’ block. This was not the case for the sequences with TR of 0.5 and 0.75 seconds. We found no difference in the time it takes for the signal from each sequence to reach the peak value of activation.

Having established that the modulation of a single brain region in neurofeedback studies has an impact not only in the target region but also on a network of regions, neuroimaging studies move towards studying the connectivity between nodes of these networks (Ramot and Martin, 2022). In this sense, if one aims to use neurofeedback to target a specific function or behavior, one should characterize the functional network involved and the appropriate target region, assess if the changes we may be inducing are propagating along the rest of the network, or even if we should be targeting some parameter of the network itself.

Here, we explore the interhemispheric functional connectivity of a region that responds to our stimuli, assessing its potential as a target for neuromodulation at different TRs. This has been successfully applied before in other neurofeedback paradigms (Pereira et al., 2019; Wang et al., 2020; Hayashi et al., 2022). Specifically, we simulated the feedback of the perceptual switches based on the hMT + interhemispheric correlation value. We found that the feedback information is both more reliable and more responsive for the higher resolution sequences (Figs. 7 and 8) when we consider a simple rule for determining a perceptual switch. Based on a previous study, which found that the more information available to the participant during neurofeedback, the greater its ability to self-regulate brain activity (Sorger et al., 2018), we conclude that the time delay between the modulation and the feedback of that modulation time is an important factor in neurofeedback paradigms. As such, if the goal is to provide feedback based on connectivity, one could consider using higher temporal resolution sequences.

Trade-offs, limitations and compromises

The neural processes indirectly inferred using fMRI vary in the scale of the millisecond but are sampled in the scale of the second. This represents a severe downsampling with fMRI sample intervals typically ranging from 1 to 3 s, way longer than typical interneuron delays (Seth, Chorley and Barnett, 2013). Nevertheless, this measure of neuronal activity can be interpreted as a representation of a low pass filter of the local field potentials, showing that neural patterns can also be found in the BOLD signal, a particularly relevant feature for connectivity methods applied to fMRI data (Fernandes et al., 2020). While the temporal resolution of this neuroimaging technique is far from others, such as electroencephalography, lowering the TR can provide us with a better sampling of the HRF and more certainty when studying brain connectivity with functional MRI.

Increasing the temporal resolution during real-time acquisitions poses challenges both in image quality and technical implementations. As recent research suggests, multiband sequences may diminish the detection ability of activity in mesolimbic regions (Srirangarajan et al., 2021) but not in other regions in the brain, as we have seen here with hMT+. Also, the temporal SNR is not homogeneous in the whole brain and tends to be lower with higher multiband factors (Todd et al., 2016; Srirangarajan et al., 2021). Hence, the recommendation for the use of these sequences for real-time fMRI is highly dependent on the target region or network of interest.

From the technical point of view, fMRI neurofeedback has high computational requirements, namely regarding image reconstruction at the scanner, network capacity and speed for image transfer at every volume, and the real-time image processing software itself. Some of these requirements have been addressed in (Renz et al., 2023), where the authors managed to achieve a stable real-time acquisition with a TR of 1 second, but not less, a result which may be highly dependent on each site’s MRI setup and infrastructure.

In conclusion, our study generalizes the hypothesis that interhemispheric connectivity reflects spontaneous perceptual switches in perceptual coherence, which is shown across temporal resolutions (even at 3T). We found stable activation metrics in the hMT + region across resolutions and consistent results of changes in interhemispheric connectivity as a function of perceptual decision, affirming the reliability of fMRI for studying dynamic connectivity patterns. While simulating a feedback signal based on interhemispheric connectivity, higher resolution sequences (TRs within 1 second and lower) showed benefits. Overall, integrating fast fMRI sequences may offer promising avenues for optimizing cognitive functions within neurofeedback settings.

Data and code availability

All the code for the above-mentioned analyses and data (including the activation maps and hMT+ timecourses) can be found at https://github.com/alexsayal/vpmb-tr.

Author contributions – AS, TS and MCB designed the study ,BD, TS and MCB provided supervision, AS acquired and analysed the data, SA acquired the data, AS wrote the first draft of the manuscript, all authors revised, edited and approved the final version.

Competing interests – the authors report no competing interests

Funding: This research work was funded by the Portuguese Foundation for Science and Technology (FCT) (grants: UID/04950B/2020, UID/04950P/2020, DSAIPA/DS/0041/2020, PTDC/PSI-GER/1326/2020, 2022.02963.PTDC – Hallucin and by the BIAL Foundation project 207/16.

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No competing interests reported.

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Interhemispheric connectivity during spontaneous switches in visual perceptual coherence as revealed by fMRI at multiple temporal resolutions

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