Spatial attention is discontinuous, sampling behaviorally relevant locations in theta-rhythmic cycles (3-6 Hz). Underlying this rhythmic sampling are intrinsic theta oscillations in frontal and ...parietal cortices that provide a clocking mechanism for two alternating attentional states that are associated with either engagement at the presently attended location (and enhanced perceptual sensitivity) or disengagement (and diminished perceptual sensitivity). It has remained unclear, however, how these theta-dependent states are coordinated across the large-scale network that directs spatial attention. The pulvinar is a candidate for such coordination, having been previously shown to regulate cortical activity. Here, we examined pulvino-cortical interactions during theta-rhythmic sampling by simultaneously recording from macaque frontal eye fields (FEF), lateral intraparietal area (LIP), and pulvinar. Neural activity propagated from pulvinar to cortex during periods of engagement, and from cortex to pulvinar during periods of disengagement. A rhythmic reweighting of pulvino-cortical interactions thus defines functional dissociations in the attention network.
Selective attention mechanisms route behaviorally relevant information through large-scale cortical networks. Although evidence suggests that populations of cortical neurons synchronize their ...activity to preferentially transmit information about attentional priorities, it is unclear how cortical synchrony across a network is accomplished. Based on its anatomical connectivity with the cortex, we hypothesized that the pulvinar, a thalamic nucleus, regulates cortical synchrony. We mapped pulvino-cortical networks within the visual system, using diffusion tensor imaging, and simultaneously recorded spikes and field potentials from these interconnected network sites in monkeys performing a visuospatial attention task. The pulvinar synchronized activity between interconnected cortical areas according to attentional allocation, suggesting a critical role for the thalamus not only in attentional selection but more generally in regulating information transmission across the visual cortex.
Brain networks are commonly defined using correlations between blood oxygen level-dependent (BOLD) signals in different brain areas. Although evidence suggests that gamma-band (30–100 Hz) neural ...activity contributes to local BOLD signals, the neural basis of interareal BOLD correlations is unclear. We first defined a visual network in monkeys based on converging evidence from interareal BOLD correlations during a fixation task, task-free state, and anesthesia, and then simultaneously recorded local field potentials (LFPs) from the same four network areas in the task-free state. Low-frequency oscillations (<20 Hz), and not gamma activity, predominantly contributed to interareal BOLD correlations. The low-frequency oscillations also influenced local processing by modulating gamma activity within individual areas. We suggest that such cross-frequency coupling links local BOLD signals to BOLD correlations across distributed networks.
► Simultaneous multiple-electrode recordings from a thalamo-cortical network ► Low-frequency neural oscillations contributed to interareal BOLD correlations ► Low-frequency oscillations modulated local gamma-frequency neural activity ► Cross-frequency coupling linked local BOLD activations to BOLD connectivity
The neural dynamics giving rise to brain networks defined by fMRI are unclear. Wang et al. show that network interactions measured using fMRI reflect low-frequency neural activity. Through cross-frequency coupling, these large-scale interactions coordinate local processes operating at high frequencies.
The pulvinar is the largest nucleus in the primate thalamus and contains extensive, reciprocal connections with visual cortex. Although the anatomical and functional organization of the pulvinar has ...been extensively studied in old and new world monkeys, little is known about the organization of the human pulvinar. Using high-resolution functional magnetic resonance imaging at 3 T, we identified two visual field maps within the ventral pulvinar, referred to as vPul1 and vPul2. Both maps contain an inversion of contralateral visual space with the upper visual field represented ventrally and the lower visual field represented dorsally. vPul1 and vPul2 border each other at the vertical meridian and share a representation of foveal space with iso-eccentricity lines extending across areal borders. Additional, coarse representations of contralateral visual space were identified within ventral medial and dorsal lateral portions of the pulvinar. Connectivity analyses on functional and diffusion imaging data revealed a strong distinction in thalamocortical connectivity between the dorsal and ventral pulvinar. The two maps in the ventral pulvinar were most strongly connected with early and extrastriate visual areas. Given the shared eccentricity representation and similarity in cortical connectivity, we propose that these two maps form a distinct visual field map cluster and perform related functions. The dorsal pulvinar was most strongly connected with parietal and frontal areas. The functional and anatomical organization observed within the human pulvinar was similar to the organization of the pulvinar in other primate species.
The anatomical organization and basic response properties of the visual pulvinar have been extensively studied in nonhuman primates. Yet, relatively little is known about the functional and anatomical organization of the human pulvinar. Using neuroimaging, we found multiple representations of visual space within the ventral human pulvinar and extensive topographically organized connectivity with visual cortex. This organization is similar to other nonhuman primates and provides additional support that the general organization of the pulvinar is consistent across the primate phylogenetic tree. These results suggest that the human pulvinar, like other primates, is well positioned to regulate corticocortical communication.
The human insular cortex is a heterogeneous brain structure which plays an integrative role in guiding behavior. The cytoarchitectonic organization of the human insula has been investigated over the ...last century using postmortem brains but there has been little progress in noninvasive in vivo mapping of its microstructure and large-scale functional circuitry. Quantitative modeling of multi-shell diffusion MRI data from 413 participants revealed that human insula microstructure differs significantly across subdivisions that serve distinct cognitive and affective functions. Insular microstructural organization was mirrored in its functionally interconnected circuits with the anterior cingulate cortex that anchors the salience network, a system important for adaptive switching of cognitive control systems. Furthermore, insular microstructural features, confirmed in Macaca mulatta, were linked to behavior and predicted individual differences in cognitive control ability. Our findings open new possibilities for probing psychiatric and neurological disorders impacted by insular cortex dysfunction, including autism, schizophrenia, and fronto-temporal dementia.
The pulvinar influences communication between cortical areas. We use fMRI to characterize the functional organization of the human pulvinar and its coupling with cortex. The ventral pulvinar is ...sensitive to spatial position and moment-to-moment transitions in visual statistics, but also differentiates visual categories such as faces and scenes. The dorsal pulvinar is modulated by spatial attention and is sensitive to the temporal structure of visual input. Cortical areas are functionally coupled with discrete pulvinar regions. The spatial organization of this coupling reflects the functional specializations and anatomical distances between cortical areas. The ventral pulvinar is functionally coupled with occipital-temporal cortices. The dorsal pulvinar is functionally coupled with frontal, parietal, and cingulate cortices, including the attention, default mode, and human-specific tool networks. These differences mirror the principles governing cortical organization of dorsal and ventral cortical visual streams. These results provide a functional framework for how the pulvinar facilitates and regulates cortical processing.
The dorsal frontoparietal attention network has been subdivided into at least eight areas in humans. However, the circuitry linking these areas and the functions of different circuit paths remain ...unclear. Using a combination of neuroimaging techniques to map spatial representations in frontoparietal areas, their functional interactions, and structural connections, we demonstrate different pathways across human dorsal frontoparietal cortex for the control of spatial attention. Our results are consistent with these pathways computing object-centered and/or viewer-centered representations of attentional priorities depending on task requirements. Our findings provide an organizing principle for the frontoparietal attention network, where distinct pathways between frontal and parietal regions contribute to multiple spatial representations, enabling flexible selection of behaviorally relevant information.
•Auditory and visual tool information are processed in separate human brain networks.•Left parietal cortex contains visual and auditory tool-specific sub-regions.•Left parietal sub-regions can decode ...tool category information across senses.•Human parietal cortex is critical in complex higher-order object processing.
Left parietal cortex has been associated with the human-specific ability of sophisticated tool use. Yet, it is unclear how tool information is represented across senses. Here, we compared auditory and visual tool-specific activations within healthy human subjects to probe the relation of tool-specific networks, uni- and multisensory response properties, and functional and structural connectivity using functional and diffusion-weighted MRI. In each subject, we identified an auditory tool network with regions in left anterior inferior parietal cortex (aud-aIPL), bilateral posterior lateral sulcus, and left inferior precentral sulcus, and a visual tool network with regions in left aIPL (vis-aIPL) and bilateral inferior temporal gyrus. Aud-aIPL was largely separate and anterior/inferior from vis-aIPL, with varying degrees of overlap across subjects. Both regions displayed a strong preference for tools versus other stimuli presented within the same modality. Despite their modality preference, aud-aIPL and vis-aIPL and a region in left inferior precentral sulcus displayed multisensory response properties, as revealed in multivariate analyses. Thus, two largely separate tool networks are engaged by the visual and auditory modalities with nodes in parietal and prefrontal cortex potentially integrating information across senses. The diversification of tool processing in human parietal cortex underpins its critical role in complex object processing.
The pulvinar is the largest nucleus in the primate thalamus and has topographically organized connections with multiple cortical areas, thereby forming extensive cortico‐pulvino‐cortical input–output ...loops. Neurophysiological studies have suggested a role for these transthalamic pathways in regulating information transmission between cortical areas. However, evidence for a causal role of the pulvinar in regulating cortico–cortical interactions is sparse and it is not known whether pulvinar's influences on cortical networks are task‐dependent or, alternatively, reflect more basic large‐scale network properties that maintain functional connectivity across networks regardless of active task demands. In the current study, under passive viewing conditions, we conducted simultaneous electrophysiological recordings from ventral (area V4) and dorsal (lateral intraparietal area LIP) nodes of macaque visual system, while reversibly inactivating the dorsal part of the lateral pulvinar (dPL), which shares common anatomical connectivity with V4 and LIP, to probe a causal role of the pulvinar. Our results show a significant reduction in local field potential phase coherence between LIP and V4 in low frequencies (4–15 Hz) following muscimol injection into dPL. At the local level, no significant changes in firing rates or LFP power were observed in LIP or in V4 following dPL inactivation. Synchronization between pulvinar spikes and cortical LFP phase decreased in low frequencies (4–15 Hz) both in LIP and V4, while the low frequency synchronization between LIP spikes and pulvinar phase increased. These results indicate a causal role for pulvinar in synchronizing neural activity between interconnected cortical nodes of a large‐scale network, even in the absence of an active task state.
The fundamental receptive field (RF) architecture in human visual cortex becomes adult-like by age 5. However, visuo-spatial functions continue to develop until teenage years. This suggests that, ...despite the early maturation of the RF structure, functional interactions within and across RFs may mature slowly. Here, we used fMRI to investigate functional interactions among multiple stimuli in the visual cortex of school children (ages 8 to 12) in the context of biased competition theory. In the adult visual system, multiple objects presented in the same visual field compete for neural representation. These competitive interactions occur at the level of the RF and are therefore closely linked to the RF architecture. Like in adults, we found suppression of evoked responses in children's visual cortex when multiple stimuli were presented simultaneously. Such suppression effects were modulated by the spatial distance between the stimuli as a function of RF size across the visual system. Our findings suggest that basic competitive interactions in the visual cortex of children above age 8 operate in an adult-like manner, with subtle differences in early visual areas and area MT. Our study establishes a paradigm and provides baseline data to investigate the neural basis of visuo-spatial processing in typical and atypical development.
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