Convergence of prefrontal and parietal anatomical projections in a connectional hub in the striatum

• Published in: NeuroImage (Orlando, Fla.) Vol. 146; pp. 821 - 832
• Main Authors: Choi, Eun Young, Tanimura, Yoko, Vage, Priti R., Yates, Ellen H., Haber, Suzanne N.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.02.2017; Elsevier Limited
• Subjects: Addictions; Adult; Anatomy; Animals; Anterior commissure; Attention; Behavior disorders; Bias; Brain Mapping; Brain research; Caudate Nucleus - cytology; Caudate Nucleus - physiology; Cognitive ability; Convergence; Corticostriatal connectivity; Drug addiction; Environmental effects; Female; Functional magnetic resonance imaging; Humans; Macaca fascicularis; Macaca mulatta; Macaca nemestrina; Magnetic Resonance Imaging; Male; Medical imaging; Mental disorders; Monkey anatomy; Neostriatum; Neural networks; Neural Pathways - cytology; Neural Pathways - physiology; Neuroanatomical Tract-Tracing Techniques; Neurological diseases; Obsessive compulsive disorder; Parietal; Parietal Lobe - cytology; Parietal Lobe - physiology; Post traumatic stress disorder; Prefrontal; Prefrontal cortex; Prefrontal Cortex - cytology; Prefrontal Cortex - physiology; Reinforcement; Resting-state functional connectivity; Striatum; Visual cortex; Visual perception; Visual task performance; Young Adult; Striatum; Resting-state functional connectivity; rdCaud; Prefrontal; Parietal; Monkey anatomy; Corticostriatal connectivity; fcMRI; vCaud
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2016.09.037

Visual attentional bias forms for rewarding and punishing stimuli in the environment. While this attentional bias is adaptive in healthy situations, it is maladaptive in disorders such as drug addiction or PTSD. In both these disorders, the ability to exert control over this attentional bias is associated with drug abstinence rates or reduced PTSD symptoms, indicating the interaction of visual attention, cognitive control, and stimulus association. The inferior parietal lobule (IPL) is central to attention, while the prefrontal cortex (PFC) is critical for reward, cognitive control, and attention. Importantly, regions of the IPL and PFC commonly project to the rostral dorsal caudate (rdCaud) of the striatum. We propose an anatomical network architecture in which IPL projections converge with PFC projections in a connectional hub in the rdCaud, providing an anatomical substrate for the interaction of these projections and their competitive influence on striatal processing. To investigate this, we mapped the dense projections from the caudal IPL and prefrontal (dlPFC, vlPFC, OFC, dACC, and dmPFC) regions that project to the medial rdCaud with anatomical tract-tracing tracer injections in monkeys. These inputs converge in a precise site in the medial rdCaud, rostral to the anterior commissure. Small retrograde tracer injections confirmed these inputs to the medial rdCaud and showed that a proximal ventral striatal location has a very different pattern of cortical inputs. We next used human resting-state functional connectivity MRI (fcMRI) to examine whether a striatal hub exists in the human medial rdCaud. Seed regions in the human medial rdCaud revealed cortical correlation maps similar to the monkey retrograde injection results. A subsequent analysis of these correlated cortical regions showed that their peak correlation within the striatum is in the medial rdCaud, indicating that this is a connectional hub. In contrast, this peak striatal correlation was not found in the ventral striatal location, suggesting that this site is not a connectional hub of cortical regions. Taken together, this work uses the precision of monkey anatomy to identify a connectional hub of IPL and PFC projections in the medial rdCaud. It also translates this anatomical precision to humans, demonstrating that, guided by anatomy, connectional hubs can be identified in humans with fcMRI. These connectional hubs provide more specific treatment targets for drug addiction, PTSD, and other neurological and psychiatric disorders involving the striatum. [Display omitted] •An anatomical architecture of a corticostriatal connectional hub is demonstrated.•Specific prefrontal and parietal projections converge in a rostral dorsal caudate hub.•Guided by anatomy, this hub is identified in humans with resting-state fcMRI.•This hub may underlie the control of attentional bias in psychiatric diseases.•Connectional hubs provide insights into specific treatment targets.