The organization of the human striatum estimated by intrinsic functional connectivity

Abstract

Choi EY, Yeo BT, Buckner RL. The organization of the human striatum estimated by intrinsic functional connectivity. J Neurophysiol 108: 2242-2263, 2012. First published July 25, 2012 doi:10.1152/jn.00270.2012.-The striatum is connected to the cerebral cortex through multiple anatomical loops that process sensory, limbic, and heteromodal information. Tract-tracing studies in the monkey reveal that these corticostriatal connections form stereotyped patterns in the striatum. Here the organization of the striatum was explored in the human with resting-state functional connectivity MRI (fcMRI). Data from 1,000 subjects were registered with nonlinear deformation of the striatum in combination with surface-based alignment of the cerebral cortex. fcMRI maps derived from seed regions placed in the foot and tongue representations of the motor cortex yielded the expected inverted somatotopy in the putamen. fcMRI maps derived from the supplementary motor area were located medially to the primary motor representation, also consistent with anatomical studies. The topography of the complete striatum was estimated and replicated by assigning each voxel in the striatum to its most strongly correlated cortical network in two independent groups of 500 subjects. The results revealed at least five cortical zones in the striatum linked to sensorimotor, premotor, limbic, and two association networks with a topography globally consistent with monkey anatomical studies. The majority of the human striatum was coupled to cortical association networks. Examining these association networks further revealed details that fractionated the five major networks. The resulting estimates of striatal organization provide a reference for exploring how the striatum contributes to processing motor, limbic, and heteromodal information through multiple large-scale corticostriatal circuits. somatotopy; limbic network; prefrontal cortex; association cortex; fMRI; functional connectivity; default network ANIMAL STUDIES and human patient cases demonstrate that the basal ganglia are involved in diverse functional domains including movement, cognition, and reward (Alexander et al. 1986;DeLong and Georgopoulos 1981;Haber and Gdowski 2004;MacLean 1972). Providing an anatomical basis for functional diversity, tract-tracing studies show that the basal ganglia are connected to distributed regions of the cerebral cortex through multiple, partially parallel anatomical loops (Alexander et al. 1986(Alexander et al. , 1990. Each loop includes projections from the cerebral cortex, through the basal ganglia, to the thalamus, and back to the cerebral cortex. Cortical efferents to the striatum (the main input nucleus of the basal ganglia) form distinct patterns depending on their cortical origin. The posterior putamen and the dorsolateral anterior putamen receive projections from motor and motor association cortex, the central anterior striatum from cognitive regions including prefrontal cortex, and the ventral anterior striatum from regions associated with the limbic syste...

Striatal subdivisions that coherently interact with multiple cerebrocortical networks

“…Supporting Information Figure S4a shows group average maps of the SSCs that were most strongly connected with the PCG, MFG, OFG, or inferior parietal lobule, based on the atlas by Desikan et al (2006). Consistent with previous studies (Barnes et al, 2010; Choi et al, 2012; Di Martino et al, 2008; Draganski et al, 2008; Garcia‐Garcia et al, 2018; Janssen et al, 2015; Jaspers et al, 2017; Jung et al, 2014), the middle part of the putamen was most strongly connected with the PCG, the caudate nucleus was most strongly connected with the MFG, and the caudate nucleus extending to ventral striatum was most strongly connected with the OFG.…”

“…Consistent with a previous study (Choi et al, 2012), the ventral part of the putamen was most strongly connected with the SM network, the dorsal part of the putamen was connected most strongly with the VA network, the caudate nucleus was most strongly connected with the FP network, and the caudate nucleus extending to the ventral striatum was most strongly connected with the Lim network. These results confirmed the larger‐scale functional organization of the striatum.…”

“…Previous studies of striatal functional architecture have revealed a well‐organized relationship for cerebrocortical‐striatal connectivity (Barnes et al, 2010; Choi et al, 2012; Di Martino et al, 2008; Draganski et al, 2008; Garcia‐Garcia et al, 2018; Janssen et al, 2015; Jaspers et al, 2017; Jung et al, 2014). We confirmed, as a positive control, that the larger‐scale observations could be replicated using the present data set.…”

How networks communicate: propagation patterns in spontaneous brain activity

“…Biswal et al used human rs-fMRI to discover that spontaneous infraslow (less than 0.1 Hz) fluctuations of the BOLD signal are highly correlated within the somatomotor system [12]. This basic result has since been extended to multiple functional networks spanning the entire brain ( [13][14][15][16][17]; figure 1a,b). Spatial correlations within intrinsic activity are widely referred to as functional connectivity; the associated topographies are known as resting state networks (RSNs [2]).…”

Targeted ablation of cholinergic interneurons in the dorsolateral striatum produces behavioral manifestations of Tourette syndrome

“…The striatum is reduced in volume in individuals with TS (12)(13)(14), and this reduction predicts the severity and the persistence of symptoms (15). Whereas the cellular architecture of the dorsal striatum is fairly uniform throughout its medial-lateral extent, the topographic organization of cortical afferents leads to functional segregation among subregions (16)(17)(18)(19). The dorsolateral striatum (DLS), which corresponds roughly to the human putamen, has been associated with sensorimotor habits (20) and with tic-like stereotypies in rodents (21,22).…”