Comparative diffusion tractography of corticostriatal motor pathways reveals differences between humans and macaques

Abstract

The primate corticobasal ganglia circuits are understood to be segregated into parallel anatomically and functionally distinct loops. Anatomical and physiological studies in macaque monkeys are summarized as showing that an oculomotor loop begins with projections from the frontal eye fields (FEF) to the caudate nucleus, and a motor loop begins with projections from the primary motor cortex (M1) to the putamen. However, recent functional and structural neuroimaging studies of the human corticostriatal system report evidence inconsistent with this organization. To obtain conclusive evidence, we directly compared the pattern of connectivity between cortical motor areas and the striatum in humans and macaques in vivo using probabilistic diffusion tractography. In macaques we found that FEF is connected with the head of the caudate and anterior putamen, and M1 is connected with more posterior sections of the caudate and putamen, corroborating neuroanatomical tract tracing findings. However, in humans FEF and M1 are connected to largely overlapping portions of posterior putamen and only a small portion of the caudate. These results demonstrate that the corticobasal connectivity for the oculomotor and primary motor loop is not entirely segregated for primates at a macroscopic level and that the description of the anatomical connectivity of corticostriatal motor systems in humans does not parallel that of macaques, perhaps because of an expansion of prefrontal projections to striatum in humans.

Speed of saccade execution and inhibition associated with fractional anisotropy in distinct fronto‐frontal and fronto‐striatal white matter pathways

“…First, although FA is the most commonly used measure of white matter integrity, it is influenced by a range of biological factors, including myelination, axonal r White Matter Integrity and Cognitive Control Speed r r 2819 r damage, axonal diameter, and fiber coherence [Assaf and Pasternak, 2008] Thus, the precise physiological underpinnings of the current findings cannot be specified; however, since this is a group of healthy, young participants, we find it unlikely that individual differences in axonal damage are driving behavioral correlations. The tracts connecting cortical regions with caudate and putamen were largely overlapping, consistent with a recent study comparing these tracts between macaques and humans [Neggers et al, 2015]. That is, we cannot say whether behavior is related to connections from region A to region B, from region B to region A, or both.…”

“…Interestingly, this overlap in connections r White Matter Integrity and Cognitive Control Speed r r 2815 r between cortex and PUT and CN dovetails with a recent study from Neggers et al [2015] who found that DTI tracts from the FEF terminated both in PUT and CN (with a dominance for PUT in humans), a finding contradicting the classically held view of the CN as oculomotor striatum [Alexander et al, 1986]. For example, the size of the seed ROI plays an important role in determining connectivity values.…”

“…To transform the ROIs into each subject's native space, the anatomical T 1 -weighted volume was realigned to the mean b0-weighted image and subsequently normalized to MNI-space using the unified segmentation algorithm as implemented in SPM8 [Ashburner and Friston, 2005]. The inverse warping parameters from this step were used to transform ROIs from MNI space to native space [see Neggers et al, 2015 for detailed methods].…”

The Crossed Projection to the Striatum in Two Species of Monkey and in Humans: Behavioral and Evolutionary Significance

“…Rilling et al (2008) described an enhanced frontotemporal component of the arcuate fasciculus in humans, possibly related to language functions. Neggers et al (2015) described more extensive overlap between eye field and M1 projections to the striatum in humans than in monkey.…”

Negative childhood experiences alter a prefrontal‐insular‐motor cortical network in healthy adults: A preliminary multimodal rsfMRI‐fMRI‐MRS‐dMRI study

“…4; Table II). However this might be related to the fact that these connections are mainly indirect through corticostriatal-motor and cortico-thalamic pathways [Guye et al, 2003;Neggers et al, 2015]. Also, the insula is anatomically variable [Rosen et al, 2015] and its connections are regionally-selective (e.g.…”