Fronto-striatal connections in the human brain: A probabilistic diffusion tractography study

Abstract

Anatomical studies in animals have described multiple striatal circuits and suggested that subcomponents of the striatum, although functionally related, project to distinct cortical areas. To date, anatomical investigations in humans have been limited by methodological constraints such that most of our knowledge of fronto-striatal networks relies on nonhuman primate studies. To better identify the fronto-striatal pathways in the human brain, we used Diffusion Tensor Imaging (DTI) tractography to reconstruct neural connections between the frontal cortex and the caudate nucleus and putamen in vivo. We demonstrate that the human caudate nucleus is interconnected with the prefrontal cortex, inferior and middle temporal gyrus, frontal eye fields, cerebellum and thalamus; the putamen is interconnected with the prefrontal cortex, primary motor area, primary somatosensory cortex, supplementary motor area, premotor area, cerebellum and thalamus. A connectivity-based seed classification analysis identified connections between the dorsolateral prefrontal areas (DLPFC) and the dorsal-posterior caudate nucleus and between the ventrolateral prefrontal areas (VLPFC) and the ventral-anterior caudate nucleus. For the putamen, connections exist between the supplementary motor area (SMA) and dorsal-posterior putamen while the premotor area projects to medial putamen, and the primary motor area to the lateral putamen. Identifying the anatomical organization of the fronto-striatal network has important implications for understanding basal ganglia function and associated disease processes. KeywordsCaudate; Putamen; Frontal connectivity; Motor connectivity; Diffusion tensor imaging (DTI) tractography; HumansThe striatum is the main entry point of cortical information to the basal ganglia and it receives afferents from anatomically and functionally different areas of the cerebral cortex.According to the current model of basal ganglia function, cortical information is processed in the basal ganglia nuclei, which in turn send projections back via the thalamus to the cortex ('cortico-basal ganglia loop') [2,1]. To date, there are two opposing views regarding

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“…Striato-cortico-striatal loops predominantly involving prefrontal cortex (PFC) projections have been delineated in nonhuman primates (Alexander et al, 1986), and confirmed in humans with diffusion tensor imaging (Leh et al, 2007;Lehericy et al, 2004) and resting-state functional magnetic resonance imaging (rs-fMRI) (Di Martino et al, 2008). These loops include: a ventral circuit anchored in the inferior limbic subdivision of the striatum and comprising connections with orbitofrontal cortex (OFC), ventromedial PFC, medial thalamus, and limbic regions that is fundamental to associative learning and reward-mediated decision making (Knutson and Cooper, 2005); and a dorsal circuit, including the associative subdivision of the striatum, dorsolateral PFC and mediodorsal and ventroanterior thalamus that maintains information relating to reward outcomes (O' Doherty et al, 2004).…”

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