Neuropsychological evidence of multi-domain network hubs in the human thalamus
- University of Iowa, United States
- The University of Sydney, Australia
Abstract
Hubs in the human brain support behaviors that arise from brain network interactions. Previous studies have identified hub regions in the human thalamus that are connected with multiple functional networks. However, the behavioral significance of thalamic hubs has yet to be established. Our framework predicts that thalamic subregions with strong hub properties are broadly involved in functions across multiple cognitive domains. To test this prediction, we studied human patients with focal thalamic lesions in conjunction with network analyses of the human thalamocortical functional connectome. In support of our prediction, lesions to thalamic subregions with stronger hub properties were associated with widespread deficits in executive, language, and memory functions, whereas lesions to thalamic subregions with weaker hub properties were associated with more limited deficits. These results highlight how a large-scale network model can broaden our understanding of thalamic function for human cognition.
Data availability
We have made all code and lesion-derived measures used in the manuscript freely available on github (https://github.com/kaihwang/LTH), including neuropsych assessment outcome, derivatives from lesion analyses, data used for functional connectivity analyses, and mRNA expression analyses. Functional connectivity analyses utilized publicly available datasets (Holmes et al., 2015; Nooner et al., 2012). The only data that we cannot post without restrictions are each patient's clinical MRI data and lesion data. Patients were enrolled into the Iowa Lesion Patient Registry the past few decades, and most did not consent to post their clinical MRI data publicly. To gain access to those data, the interested party will have to contact the PI of the lesion registry, Dr. Dan Tranel, and the corresponding author of this project, Dr. Kai Hwang. The user will require to sign a data use agreement. This institutional policy was designed to ensure the appropriate use of the data for academic and not commercial purposes. A study plan of the proposed research will have to be submitted, and we will work with the interested party to obtain the necessary IRB approval from both institutions.
-
Brain Genomics Superstruct ProjectBrain Genomics Superstruct Project initial data release with structural, functional, and behavioral measures.
-
NKI-Rockland sampleThe enhanced Nathan Kline Institute-Rockland Sample (NKI-RS).
Article and author information
Author details
Funding
National Institutes of Health (R01MH122613)
- Kai Hwang
- Daniel Tranel
- Aaron Boes
National Institutes of Health (RO1MH117772)
- James M Shine
National Institutes of Health (P50MH094258)
- Daniel Tranel
Kiwanis Neuroscience Research Foundation
- Daniel Tranel
National Institutes of Health (R01NS114405)
- Aaron Boes
National Institutes of Health (R21MH120441)
- Aaron Boes
National Health and Medical Research Council (GNT1156536)
- James M Shine
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: All participants gave written informed consent, and the study was approved by the University of Iowa Institutional Review Board (protocol #200105018).
Copyright
© 2021, Hwang et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 1,675
- views
-
- 288
- downloads
-
- 36
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Neuropsychological evidence of multi-domain network hubs in the human thalamus
eLife 10:e69480.
https://doi.org/10.7554/eLife.69480
Further reading
-
- Neuroscience
Studying infant minds with movies is a promising way to increase engagement relative to traditional tasks. However, the spatial specificity and functional significance of movie-evoked activity in infants remains unclear. Here, we investigated what movies can reveal about the organization of the infant visual system. We collected fMRI data from 15 awake infants and toddlers aged 5–23 months who attentively watched a movie. The activity evoked by the movie reflected the functional profile of visual areas. Namely, homotopic areas from the two hemispheres responded similarly to the movie, whereas distinct areas responded dissimilarly, especially across dorsal and ventral visual cortex. Moreover, visual maps that typically require time-intensive and complicated retinotopic mapping could be predicted, albeit imprecisely, from movie-evoked activity in both data-driven analyses (i.e. independent component analysis) at the individual level and by using functional alignment into a common low-dimensional embedding to generalize across participants. These results suggest that the infant visual system is already structured to process dynamic, naturalistic information and that fine-grained cortical organization can be discovered from movie data.
-
- Neuroscience
Memory consolidation during sleep depends on the interregional coupling of slow waves, spindles, and sharp wave-ripples (SWRs), across the cortex, thalamus, and hippocampus. The reuniens nucleus of the thalamus, linking the medial prefrontal cortex (mPFC) and the hippocampus, may facilitate interregional coupling during sleep. To test this hypothesis, we used intracellular, extracellular unit and local field potential recordings in anesthetized and head restrained non-anesthetized cats as well as computational modelling. Electrical stimulation of the reuniens evoked both antidromic and orthodromic intracellular mPFC responses, consistent with bidirectional functional connectivity between mPFC, reuniens and hippocampus in anesthetized state. The major finding obtained from behaving animals is that at least during NREM sleep hippocampo-reuniens-mPFC form a functional loop. SWRs facilitate the triggering of thalamic spindles, which later reach neocortex. In return, transition to mPFC UP states increase the probability of hippocampal SWRs and later modulate spindle amplitude. During REM sleep hippocampal theta activity provides periodic locking of reuniens neuronal firing and strong crosscorrelation at LFP level, but the values of reuniens-mPFC crosscorrelation was relatively low and theta power at mPFC was low. The neural mass model of this network demonstrates that the strength of bidirectional hippocampo-thalamic connections determines the coupling of oscillations, suggesting a mechanistic link between synaptic weights and the propensity for interregional synchrony. Our results demonstrate the presence of functional connectivity in hippocampo-thalamo-cortical network, but the efficacy of this connectivity is modulated by behavioral state.
