Resting State Dynamic Reconfiguration of Spatial Attention Cortical Networks and Visuospatial Functioning in Non-Verbal Learning Disability (NVLD): A HD-EEG Investigation

Abstract

Nonverbal learning disability (NVLD) is a neurodevelopmental disorder characterized by deficits in visuospatial processing but spared verbal competencies. Neurocognitive markers may provide confirmatory evidence for characterizing NVLD as a separate neurodevelopmental disorder. Visuospatial performance and high-density electroencephalography (EEG) were measured in 16 NLVD and in 16 typically developing (TD) children. Cortical source modeling was applied to assess resting-state functional connectivity (rs-FC) in spatial attention networks (dorsal (DAN) and ventral attention networks (VAN)) implicated in visuospatial abilities. A machine-learning approach was applied to investigate whether group membership could be predicted from rs-FC maps and if these connectivity patterns were predictive of visuospatial performance. Graph theoretical measures were applied to nodes inside each network. EEG rs-FC maps in the gamma and beta band differentiated children with and without NVLD, with increased but more diffuse and less efficient functional connections bilaterally in the NVLD group. While rs-FC of the left DAN in the gamma range predicted visuospatial scores for TD children, in the NVLD group rs-FC of the right DAN in the delta range predicted impaired visuospatial performance, confirming that NVLD is a disorder with a predominant dysfunction in right hemisphere connectivity patterns.

Keywords: delta band; gamma band; nonverbal learning disability; resting-state electroencephalography; right hemisphere; visuospatial abilities.

Figure 4

Connectivity degree in the dorsal attention network. Node size represents the value of degree, whereas node color relates to the BF value: red for a BF > 10 and blue for a BF < 3. The red nodes report evidence for a significant difference between NVLD and TD children. (A,B): Increased connectivity degree in the bilateral intraparietal sulcus (IPS) for the NVLD group compared to TD controls, in the beta frequency band. (C,D): Increased connectivity degree for NVLD children compared to TD controls, in bilateral IPS and areas of the frontal eye field (FEF) in the right hemisphere in the gamma frequency band (see Table A1 for details on statistics).

Figure 1

Prediction of the visuospatial performance from the connectivity maps in TD children. (a): Prediction of visuospatial individual performance (as indexed by the Rey index) from rs-functional connectivity within the left dorsal attention network (DAN; R = 0.89, BF₁₀ = 2343.64) in TD children in the gamma frequency band. (b): BF robustness check showing that the evidence was preserved as extreme (BFs₁₀ > 1000) by varying the Cauchy prior width.

Figure 2

Prediction of the visuospatial performance from the connectivity maps in NVLD children. (a): Prediction of visuospatial individual performance (as indexed by the Rey index) from rs-functional connectivity within the right dorsal attention network (DAN; R = 0.84, BF₁₀ = 445.28) in NVLD children in the delta frequency band. (b): BF robustness check showing that the evidence was preserved as extreme (BF₁₀ > 100) by varying the Cauchy prior width.

Figure 3

(a): Mean global efficiency for the NVLD children, which was lower than that of the controls (BF₁₀ = 4.78) in the left VAN (in the beta frequency band). (b): BF robustness check showing that the evidence was preserved as moderate (3 < BFs_10ß < 10) by varying the Cauchy prior width.

Figure 5

Connectivity strength in the dorsal attention network. Node size represents the strength value, whereas the color relates to the BF value: red for a BF > 30 in panels (A) and (B), and BF > 4 in panels (C) and (D); blue for a BF < 3. The red nodes report evidence for a significant difference between NVLD and TD children. (A,B): Increased connectivity strength in the bilateral frontal eye field (FEF) areas within the dorsal attention network for NVLD children compared to TD controls in the beta frequency band. (C,D): Increased connectivity strength for NVLD children compared to TD controls in bilateral IPS and areas of the FEF in the right hemisphere in the gamma frequency band (see Table A2 for details on statistics).

Figure 6

Connectivity clustering in the dorsal attention network. Node size represents the clustering value, whereas node color relates to the BF value: red for a BF > 3 and blue for a BF < 3. The red nodes report evidence for a significant difference between NVLD and TD children. (A,B): Decreased clustering coefficient for NVLD children compared to TD controls, in bilateral areas of the frontal eye field (FEF) in the beta frequency band (see Table A3 for details on statistics).

Figure 7

Connectivity clustering in the ventral attention network. The node size represents the clustering value, whereas node color relates to the BF value: red for a BF > 4 in panels (A,B), BF > 7 in panels (C) and (D;) and blue for a BF < 3. The red nodes report evidence for a significant difference between NVLD and TD children. (A,B): Decreased clustering coefficient in the left frontal areas for NVLD children compared to TD controls in the beta frequency band. (C,D): Increased clustering coefficient for NVLD children compared to TD controls in areas within the right temporoparietal junction (TPJ) in the gamma frequency band (see Table A4 for details on statistics).