Functional parcellation of human and macaque striatum reveals human-specific connectivity in the dorsal caudate

Abstract

A wide homology between human and macaque striatum is often assumed as in both the striatum is involved in cognition, emotion and executive functions. However, differences in functional and structural organization between human and macaque striatum may reveal evolutionary divergence and shed light on human vulnerability to neuropsychiatric diseases. For instance, dopaminergic dysfunction of the human striatum is considered to be a pathophysiological underpinning of different disorders, such as Parkinson's disease (PD) and schizophrenia (SCZ). Previous investigations have found a wide similarity in structural connectivity of the striatum between human and macaque, leaving the cross-species comparison of its functional organization unknown. In this study, resting-state functional connectivity (RSFC) derived striatal parcels were compared based on their homologous cortico-striatal connectivity. The goal here was to identify striatal parcels whose connectivity is human-specific compared to macaque parcels. Functional parcellation revealed that the human striatum was split into dorsal, dorsomedial, and rostral caudate and ventral, central, and caudal putamen, while the macaque striatum was divided into dorsal, and rostral caudate and rostral, and caudal putamen. Cross-species comparison indicated dissimilar cortico-striatal RSFC of the topographically similar dorsal caudate. We probed clinical relevance of the striatal clusters by examining differences in their cortico-striatal RSFC and gray matter (GM) volume between patients (with PD and SCZ) and healthy controls. We found abnormal RSFC not only between dorsal caudate, but also between rostral caudate, ventral, central and caudal putamen and widespread cortical regions for both PD and SCZ patients. Also, we observed significant structural atrophy in rostral caudate, ventral and central putamen for both PD and SCZ while atrophy in the dorsal caudate was specific to PD. Taken together, our cross-species comparative results revealed shared and human-specific RSFC of different striatal clusters reinforcing the complex organization and function of the striatum. In addition, we provided a testable hypothesis that abnormalities in a region with human-specific connectivity, i.e., dorsal caudate, might be associated with neuropsychiatric disorders.

Brain intrinsic connection patterns underlying tool processing in human adults are present in neonates and not in macaques

“…The cross-species functional alignment approach we adopted here uses a joint-embedding technique that represents the functional organization of human and macaque brains in a high-dimensional common space. This method allows for cortical transformation between species, which had been suggested as the state-of-art transformation approaches (Liu et al, 2021;Van Essen et al, 2019). Direct comparisons between our transformed ROIs and the manually-drawn regions available in Howells et al, 2020 revealed overlaps between the registered frontal and parietal regions and the key components of the macaque grasping network (Figure S2), confirming the anatomical validity of the current registration approach.…”

Neural bases of Frustration-Aggression Theory: A multi-domain meta-analysis of functional neuroimaging studies

“…In our meta-analysis we found that retaliatory behaviors were mainly characterized by activation in the dorsal striatum and primary somatosensory cortex (SI, BA3 encompassing the hand network of the left hemisphere), as well as bilateral FIC and aMCC/pre-SMA. Through projections from these regions to the caudate nucleus ((Haber, 2016; Haber & Knutson, 2010; Leh, Ptito, Chakravarty, & Strafella, 2007; Xiaojin Liu et al, 2021), behavioral responses to frustration are likely to arise. Indeed, the dorsal striatum has been implicated in several goal-directed decision making and action selection and initiation (Balleine, Delgado, & Hikosaka, 2007; Haber & Knutson, 2010; O’Doherty et al, 2004).…”

Concurrent mapping of brain ontogeny and phylogeny within a common connectivity space

“…For instance, it is known that aging does not influence all brain systems equally 100 and it has been hypothesised that “evolutionary” bundles (i.e. those that are common across species but show evolutionary change) are particularly vulnerable to the effects of aging and to diseases that are uniquely human, such as schizophrenia 101,102 . Additionally, it has been argued that individual variability across human brains is found in the same places as variation across primate species 103 , presumably because evolution exploits the variation across individuals.…”