Less is more: Importance of long-range exceptions in brain architecture

Presented During:

Tuesday, June 25, 2024: 12:00 PM - 1:15 PM
COEX  
Room: Grand Ballroom 104-105  

Poster No:

1826 

Submission Type:

Abstract Submission 

Authors:

Jakub Vohryzek1, Morten Kringelbach2, Gustavo Deco3

Institutions:

1UNIVERSITAT POMPEU FABRA, Barcelona, Barcelona, 2University of Oxford, Oxford, Oxfordshire, 3Pompeu Fabra University, Barcelona, Catalonia

First Author:

Jakub Vohryzek  
UNIVERSITAT POMPEU FABRA
Barcelona, Barcelona

Co-Author(s):

Morten Kringelbach  
University of Oxford
Oxford, Oxfordshire
Gustavo Deco  
Pompeu Fabra University
Barcelona, Catalonia

Introduction:

How brain architecture shapes function is a deep question which has occupied many researchers, from the perspective of network neuroscience (Bullmore and Sporns 2009), brain modelling (Breakspear 2017) and spectral graph theory (Atasoy, Donnelly, and Pearson 2016). Some have even suggested that geometry plays a particularly relevant role in shaping functional activity (Pang et al. 2023a), although see this ongoing discussion (Faskowitz et al. 2023; Pang et al. 2023b). Here we focus on probing the importance of the rare long-range exceptions to the exponential distance rule of brain wiring (Markov et al. 2013). New evidence using turbulence has demonstrated the fundamental role of long-range connectivity in shaping optimal brain information processing (Deco et al. 2021). Here we used Laplacian decomposition of four different graph representations of the underlying anatomy to derive anatomical brain modes: exponential-distance rule (EDR) (Ercsey-Ravasz et al. 2013) and long-range exceptions (EDR+LR), geometry-based modes (geometry) and EDR modes (EDR binary and EDR continuous) (Figure 1 A). Our results show that EDR+LR achieves significantly better reconstruction of long-range functional connectivity (FC) compared to the other mode representations. Furthermore, pertinent to time-critical information processing, we show that a small subset of modes achieves a disproportionately high reconstruction of task MRI activity. When this subset of modes is considered, EDR+LR achieves better reconstruction for the 47 HCP tasks compared to the other mode representations, suggesting that less is more for information processing in the brain.

Methods:

We used publicly available data by the Human Connectome Project (HCP) of resting-state and task fMRI of 255 participants. The various modes are derived from applying the laplace decomposition on the graph representation (Figure 1 B, i). These modes are used to reconstruct the fMRI activity by a linear combination of their contributions (Figure 1 B, ii). This serves to reconstruct the resting-state fMRI activity and in particular the long-range connectivity exceptions derived as high-correlation values (<0.5 correlation) and over a long euclidean distance (<40mm) as well as the task fMRI activation maps (Figure 1 B, iii). Four different graph representations were constructed and decomposed into their associated modes (Figure 1 C). Namely, the fitted weighted and binary Euclidean Distance Rule with lambda of 0.18, EDR with long-range connectivity and the geometric modes (Pang et al. 2023a).

Results:

An important feature of cortex dynamics are long-range functional connections, defined by high correlation values (<0.5 correlation) and euclidean distance (<40mm) (Figure 2 A). We reconstructed the FC long-range connections for an increasing number of modes (1-200) showing the EDR+LR modes to have the highest reconstruction correlation (Figure 2 B). EDR+LR is statistically higher compared to the other modes (paired t-test, pval<0.05) (Figure 2 C) . For the reconstruction of the 7 activation task fMRI maps lower frequency modes contribute disproportionately more toward the reconstruction error as seen by the elbow around 20 modes (Figure 2 D). We therefore reconstructed the error for the 47 HCP tasks benchmarked against the geometrical modes for the first 20 modes (blue - better reconstruction correlation of the chosen modes, red better for the geometric modes). On average EDR+LR showed the most accurate reconstruction across tasks and number of reconstructed modes 1-20 (Figure 2 E).

Conclusions:

Here we show the importance of long-range connectivity as a key feature of shaping brain functional activity both for the spontaneous and task-based fMRI. Moreover, functional brain activity can be shown to be on a lower-dimensional manifold span by a subset of these fundamental modes with the most appropriate representation from the EDR+LR graph, suggesting that less is more for efficient information processing in the brain.

Modeling and Analysis Methods:

Connectivity (eg. functional, effective, structural) 2
fMRI Connectivity and Network Modeling 1

Keywords:

Modeling

1|2Indicates the priority used for review
Supporting Image: Figure1_OHBM2024_v1.png
Supporting Image: Figure2_OHBM2024_v1.png
 

Provide references using author date format

Atasoy, Selen, Isaac Donnelly, and Joel Pearson. 2016. “Human Brain Networks Function in Connectome-Specific Harmonic Waves.” Nature Communications 7 (1): 1–10.
Breakspear, Michael. 2017. “Dynamic Models of Large-Scale Brain Activity.” Nature Neuroscience 20 (3): 340–52.
Bullmore, Ed, and Olaf Sporns. 2009. “Complex Brain Networks: Graph Theoretical Analysis of Structural and Functional Systems.” Nature Reviews. Neuroscience 10 (3): 186–98.
Deco, Gustavo, Yonathan Sanz Perl, Peter Vuust, Enzo Tagliazucchi, Henry Kennedy, and Morten L. Kringelbach. 2021. “Rare Long-Range Cortical Connections Enhance Human Information Processing.” Current Biology: CB 31 (20): 4436–48.e5.
Ercsey-Ravasz, Mária, Nikola T. Markov, Camille Lamy, David C. Van Essen, Kenneth Knoblauch, Zoltán Toroczkai, and Henry Kennedy. 2013. “A Predictive Network Model of Cerebral Cortical Connectivity Based on a Distance Rule.” Neuron 80 (1): 184–97.
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Markov, Nikola T., Maria Ercsey-Ravasz, Camille Lamy, Ana Rita Ribeiro Gomes, Loïc Magrou, Pierre Misery, Pascale Giroud, et al. 2013. “The Role of Long-Range Connections on the Specificity of the Macaque Interareal Cortical Network.” Proceedings of the National Academy of Sciences of the United States of America 110 (13): 5187–92.
Pang, James C., Kevin M. Aquino, Marianne Oldehinkel, Peter A. Robinson, Ben D. Fulcher, Michael Breakspear, and Alex Fornito. 2023a. “Geometric Constraints on Human Brain Function.” Nature 618 (7965): 566–74.
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