The resting-state human brain networks underlie fundamental cognitive functions and consist of complex interactions among brain regions. However, the level of complexity of the resting-state networks has not been quantified, which has prevented comprehensive descriptions of the brain activity as an integrative system. Here, we address this issue by demonstrating that a pairwise maximum entropy model, which takes into account region-specific activity rates and pairwise interactions, can be robustly and accurately fitted to resting-state human brain activities obtained by functional magnetic resonance imaging. Furthermore, to validate the approximation of the resting-state networks by the pairwise maximum entropy model, we show that the functional interactions estimated by the pairwise maximum entropy model reflect anatomical connexions more accurately than the conventional functional connectivity method. These findings indicate that a relatively simple statistical model not only captures the structure of the resting-state networks but also provides a possible method to derive physiological information about various large-scale brain networks.

During rest, the human brain performs essential functions such as memory maintenance, which are associated with resting-state brain networks (RSNs) including the default-mode network (DMN) and frontoparietal network (FPN). Previous studies based on spiking-neuron network models and their reduced models, as well as those based on imaging data, suggest that resting-state network activity can be captured as attractor dynamics, i.e., dynamics of the brain state toward an attractive state and transitions between different attractors. Here, we analyze the energy landscapes of the RSNs by applying the maximum entropy model, or equivalently the Ising spin model, to human RSN data. We use the previously estimated parameter values to define the energy landscape, and the disconnectivity graph method to estimate the number of local energy minima (equivalent to attractors in attractor dynamics), the basin size, and hierarchical relationships among the different local minima. In both of the DMN and FPN, low-energy local minima tended to have large basins. A majority of the network states belonged to a basin of one of a few local minima. Therefore, a small number of local minima constituted the backbone of each RSN. In the DMN, the energy landscape consisted of two groups of low-energy local minima that are separated by a relatively high energy barrier. Within each group, the activity patterns of the local minima were similar, and different minima were connected by relatively low energy barriers. In the FPN, all dominant local minima were separated by relatively low energy barriers such that they formed a single coarse-grained global minimum. Our results indicate that multistable attractor dynamics may underlie the DMN, but not the FPN, and assist memory maintenance with different memory states.

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The orbitofrontal cortex (OFC) is involved in cognitive functions, and is also closely related to autonomic functions. The OFC is densely connected with the hypothalamus, a heterogeneous structure controlling autonomic functions that can be divided into two major parts: the lateral and the medial. Resting-state functional connectivity has allowed us to parcellate the cerebral cortex into putative functional areas based on the changes in the spatial pattern of connectivity in the cerebral cortex when a seed point is moved from one voxel to another. In the present high spatial-resolution fMRI study, we investigate the connectivity-based organization of the OFC with reference to the hypothalamus. The OFC was parcellated using resting-state functional connectivity in an individual subject approach, and then the functional connectivity was examined between the parcellated areas in the OFC and the lateral/medial hypothalamus. We found a functional double dissociation in the OFC: the lateral OFC (the lateral orbital gyrus) was more likely connected with the lateral hypothalamus, whereas the medial OFC (the medial orbital and rectal gyri) was more likely connected with the medial hypothalamus. These results demonstrate the fundamental heterogeneity of the OFC, and suggest a potential neural basis of the OFC–hypothalamic functional interaction.

Retrieval of remote memory is considered to differentially involve the anterior and posterior temporal neocortices. Previous neuropsychological studies suggest that the different posterior temporal cortical regions are involved in the retrieval of remote memory of different categories of stimuli, whereas the anterior region is involved more generally in remote memory retrieval. In the present study, using functional magnetic resonance imaging of human brains, we tested this dissociation by examining the more precise characteristics of the anterior and posterior temporal cortical regions. Two categories of stimuli, faces and scenes, were used for paired stimuli to be retrieved, and the brain activity during retrieval of paired stimuli that were learned immediately before the scanning was compared with that during retrieval of paired stimuli that were learned ϳ8 weeks earlier. We found that the different posterior temporal cortical regions were activated during retrieval of different categories of remote memory in a category-specific manner, whereas the anterior temporal cortical region was activated during retrieval of remote memory in a category-general manner. Furthermore, by applying a multivariate pattern analysis to psychophysiological interactions during retrieval of remote memory relative to recent memory, we revealed the significant interaction from the category-specific posterior temporal cortical regions to the category-general anterior temporal region. These results suggest that the posterior temporal cortical regions are involved in representation and retrieval of category-specific remote memory, whereas the anterior cortical temporal region is involved in category-general retrieval process of remote memory.

Recent advancement of resting-state functional connectivity magnetic resonance imaging (MRI) has provided a method for drawing boundaries of brain areas. However, it remains to be elucidated how the parcellated areas in the association cortex relate to the spatial extent of the brain activation which ought to reflect a functional unit in the neural network supporting that particular function. To address this issue, in the present study, we first mapped boundaries and 2 adjacent activations in the human inferior frontal cortex, and then examined the spatial relationship between the boundaries and the 2 activations. The boundaries mapped with high-resolution functional magnetic resonance imaging revealed a collection of micromodules, the size of which was approximately only 12 mm on average, much smaller than the Brodmann areas. Each of the 2 activations associated with 2 functions, response inhibition and feedback processing, was smaller in size than the micromodules. By comparing the spatial patterns between the boundaries and the 2 activations, it was revealed that the brain activations were less likely to be located on the boundaries. These results suggest the functional relevance of the areas in the association cortex delineated by the boundary mapping method based on resting-state functional connectivity MRI.

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The current data article provides behavioral and neuroimaging data for the research article "Relatedness-dependent rapid development of brain activity in anterior temporal cortex during pair-association retrieval” (Jimura et al., 2016) [1]. Behavioral performance is provided in a table. Fig. 2 of the article is based on this table. Brain regions showing time effect are provided in a table. A statistical activation map for the time effect is shown in Fig. 3C of the article.