Abstract
We investigated the anatomical and functional organization of the human substantia nigra (SN) using diffusion and functional MRI data from the Human Connectome Project. We identified a tripartite connectivity-based parcellation of SN with a limbic, cognitive, motor arrangement. The medial SN connects with limbic striatal and cortical regions and encodes value (greater response to monetary wins than losses during fMRI), while the ventral SN connects with associative regions of cortex and striatum and encodes salience (equal response to wins and losses). The lateral SN connects with somatomotor regions of striatum and cortex and also encodes salience. Behavioral measures from delay discounting and flanker tasks supported a role for the value-coding medial SN network in decisional impulsivity, while the salience-coding ventral SN network was associated with motor impulsivity. In sum, there is anatomical and functional heterogeneity of human SN, which underpins value versus salience coding, and impulsive choice versus impulsive action.
Highlights
Dopamine innervation to the cerebral hemispheres originates in the substantia nigra (SN) and ventral tegmental area (VTA) of the midbrain
Three stable subdivisions were identified in the SN of each hemisphere (Figure 2B): a dorsolateral area corresponding to lateral part of SN pars compacta, a dorsomedial area corresponding to medial part of SN pars compacta and a ventral area
This separation of dorsomedial, lateral and ventral SN coincides with descriptions of dorsal, middle and ventral tiers of midbrain dopamine cells in primates (Figure 2—figure supplement 1), which have distinct afferent and efferent striatal and cortical projections (Haber, 2014; Haber and Knutson, 2010)
Summary
Dopamine innervation to the cerebral hemispheres originates in the substantia nigra (SN) and ventral tegmental area (VTA) of the midbrain. SN/VTA dopamine neurons display variations in both anatomy and function. SN neurons can be divided into three tiers based on their staining, morphology, and connectivity with the striatum (Haber, 2014; Haber and Knutson, 2010): moving from a dorso-medial to ventro-lateral location in midbrain, dopamine neurons project to limbic, associative and motor striatum. Distinct functional characteristics have been reported for SN/VTA neurons by recording neural activity during appetitive and aversive outcomes (Matsumoto and Hikosaka, 2009; Nomoto et al, 2010). Cells in ventromedial SNc and VTA encode a value signal, being excited by appetitive events and inhibited by aversive events. Neurons in lateral SN may encode a salience signal, responding to appetitive and aversive stimuli
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