Dataset Information

Interspecies Differences in the Connectivity of Ventral Striatal Components Between Humans and Macaques.

ABSTRACT: Although the evolutionarily conserved functions of the ventral striatal components have been used as a priori knowledge for further study, whether these functions are conserved between species remains unclear. In particular, whether macroscopic connectivity supports this given the disproportionate volumetric differences between species in the brain regions that project to the ventral striatum, including the prefrontal and limbic areas, has not been established In this study, the human and macaque striatum was first tractographically parcellated to define the ventral striatum and its two subregions, the nucleus accumbens (Acb)-like and the neurochemically unique domains of the Acb and putamen (NUDAPs)-like divisions. Our results revealed a similar topographical distribution of the connectivity-based ventral striatal components in the two primate brains. Successively, a set of targets was extracted to construct a connectivity fingerprint to characterize these parcellation results, enabling cross-species comparisons. Our results indicated that the connectivity fingerprints of the ventral striatum-like divisions were dissimilar in the two species. We localized this difference to specific targets to analyze possible interspecies functional modifications. Our results also revealed interspecies-convergent connectivity ratio fingerprints of the target group to these two ventral striatum-like subregions. This convergence may suggest synchronous connectional changes of these ventral striatal components during primate evolution.

SUBMITTER: Xia X

PROVIDER: S-EPMC6587664 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Interspecies Differences in the Connectivity of Ventral Striatal Components Between Humans and Macaques.

Xia Xiaoluan X Fan Lingzhong L Cheng Chen C Yao Rong R Deng HongXia H Zhao Dongqin D Li Haifang H Jiang Tianzi T

Frontiers in neuroscience 20190614

Although the evolutionarily conserved functions of the ventral striatal components have been used as <i>a priori</i> knowledge for further study, whether these functions are conserved between species remains unclear. In particular, whether macroscopic connectivity supports this given the disproportionate volumetric differences between species in the brain regions that project to the ventral striatum, including the prefrontal and limbic areas, has not been established In this study, the human and ...[more]

PMID: 31258468

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Project description:BackgroundGrowing evidence points towards dysfunction of the ventral striatum as a neural substrate of motivational impairments in schizophrenia. Ventral striatal activity during reward anticipation is generally reduced in patients with schizophrenia and specifically correlates with apathy. However, little is known about the cortico-striatal functional connectivity in patients with schizophrenia during reward anticipation and its relation to negative symptoms.ObjectivesThe aim of this study was to identify categorical group differences in ventral striatal functional connectivity during reward anticipation between patients with schizophrenia and healthy controls, and dimensional associations between cortico-striatal functional connectivity and negative symptom severity.MethodA total of 40 patients with schizophrenia (10 females) and 33 healthy controls (8 females) were included from two previously published studies. All participants performed a variant of the Monetary Incentive Delay Task while undergoing event-related fMRI. Functional connectivity was assessed using psychophysical interactions (PPI) with the left and right ventral striatum as seeds and the contrast [High Reward Anticipation - No Reward Anticipation]. Negative symptoms were assessed using the Brief Negative Symptom Scale.ResultsCompared to controls, patients with schizophrenia showed increased functional connectivity between the left ventral striatum and the left precuneus and right parahippocampal gyrus, two hubs of the default mode network (cluster-level threshold: FWE, p < .05). In addition, we found a negative association between apathy scores on the BNSS and increased functional connectivity between the left ventral striatum and the left ventral anterior insula / putamen and the left inferior frontal gyrus / dorsal anterior insula (cluster-level threshold: FWE, p < .05).ConclusionsOur results indicate that the patterns of increased functional connectivity between the ventral striatum and the dorsal default mode network during reward anticipation could act as a compensatory mechanism to regulate the activity of the ventral striatum. Our results also showed that functional connectivity patterns from the ventral striatum, much like its local activity, is specifically related to apathy, and not diminished expression.

Project description:A subgroup of Parkinson's disease (PD) patients treated with dopaminergic therapy develop compulsive reward-driven behaviors, which can result in life-altering morbidity. The mesocorticolimbic dopamine network guides reward-motivated behavior; however, its role in this treatment-related behavioral phenotype is incompletely understood. Here, mesocorticolimbic network function in PD patients who develop impulsive and compulsive behaviors (ICB) in response to dopamine agonists was assessed using BOLD fMRI. The tested hypothesis was that network connectivity between the ventral striatum and the limbic cortex is elevated in patients with ICB and that reward-learning proficiency reflects the extent of mesocorticolimbic network connectivity. To evaluate this hypothesis, 3.0T BOLD-fMRI was applied to measure baseline functional connectivity on and off dopamine agonist therapy in age and sex-matched PD patients with (n = 19) or without (n = 18) ICB. An incentive-based task was administered to a subset of patients (n = 20) to quantify positively or negatively reinforced learning. Whole-brain voxelwise analyses and region-of-interest-based mixed linear effects modeling were performed. Elevated ventral striatal connectivity to the anterior cingulate gyrus (P = 0.013), orbitofrontal cortex (P = 0.034), insula (P = 0.044), putamen (P = 0.014), globus pallidus (P < 0.01), and thalamus (P < 0.01) was observed in patients with ICB. A strong trend for elevated amygdala-to-midbrain connectivity was found in ICB patients on dopamine agonist. Ventral striatum-to-subgenual cingulate connectivity correlated with reward learning (P < 0.01), but not with punishment-avoidance learning. These data indicate that PD-ICB patients have elevated network connectivity in the mesocorticolimbic network. Behaviorally, proficient reward-based learning is related to this enhanced limbic and ventral striatal connectivity. Hum Brain Mapp 39:509-521, 2018. © 2017 Wiley Periodicals, Inc.

Project description:UnlabelledThe existence of color-processing regions in the human ventral visual pathway (VVP) has long been known from patient and imaging studies, but their location in the cortex relative to other regions, their selectivity for color compared with other properties (shape and object category), and their relationship to color-processing regions found in nonhuman primates remain unclear. We addressed these questions by scanning 13 subjects with fMRI while they viewed two versions of movie clips (colored, achromatic) of five different object classes (faces, scenes, bodies, objects, scrambled objects). We identified regions in each subject that were selective for color, faces, places, and object shape, and measured responses within these regions to the 10 conditions in independently acquired data. We report two key findings. First, the three previously reported color-biased regions (located within a band running posterior-anterior along the VVP, present in most of our subjects) were sandwiched between face-selective cortex and place-selective cortex, forming parallel bands of face, color, and place selectivity that tracked the fusiform gyrus/collateral sulcus. Second, the posterior color-biased regions showed little or no selectivity for object shape or for particular stimulus categories and showed no interaction of color preference with stimulus category, suggesting that they code color independently of shape or stimulus category; moreover, the shape-biased lateral occipital region showed no significant color bias. These observations mirror results in macaque inferior temporal cortex (Lafer-Sousa and Conway, 2013), and taken together, these results suggest a homology in which the entire tripartite face/color/place system of primates migrated onto the ventral surface in humans over the course of evolution.Significance statementHere we report that color-biased cortex is sandwiched between face-selective and place-selective cortex on the bottom surface of the brain in humans. This face/color/place organization mirrors that seen on the lateral surface of the temporal lobe in macaques, suggesting that the entire tripartite system is homologous between species. This result validates the use of macaques as a model for human vision, making possible more powerful investigations into the connectivity, precise neural codes, and development of this part of the brain. In addition, we find substantial segregation of color from shape selectivity in posterior regions, as observed in macaques, indicating a considerable dissociation of the processing of shape and color in both species.

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Interspecies Differences in the Connectivity of Ventral Striatal Components Between Humans and Macaques.

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Interspecies Differences in the Connectivity of Ventral Striatal Components Between Humans and Macaques.

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