The cortical network that processes visual cues to self-motion was characterized with functional magnetic resonance imaging in 3 awake behaving macaques. The experimental protocol was similar to previous human studies in which the responses to a single large optic flow patch were contrasted with responses to an array of 9 similar flow patches. This distinguishes cortical regions where neurons respond to flow in their receptive fields regardless of surrounding motion from those that are sensitive to whether the overall image arises from self-motion. In all 3 animals, significant selectivity for egomotion-consistent flow was found in several areas previously associated with optic flow processing, and notably dorsal middle superior temporal area, ventral intra-parietal area, and VPS. It was also seen in areas 7a (Opt), STPm, FEFsem, FEFsac and in a region of the cingulate sulcus that may be homologous with human area CSv. Selectivity for egomotion-compatible flow was never total but was particularly strong in VPS and putative macaque CSv. Direct comparison of results with the equivalent human studies reveals several commonalities but also some differences.

Summary Monkey electrophysiology [1, 2] suggests that the activity of the ventral tegmental area (VTA) helps regulate reinforcement learning and motivated behavior, in part by broadcasting prediction-error signals throughout the reward system. However, electrophysiological studies do not allow causal inferences regarding the activity of VTA neurons with respect to these processes, as this requires artificial manipulation of neuronal firing. Rodent studies fulfilled this requirement by demonstrating that electrical and optogenetic VTA stimulation can induce learning and modulate downstream structures [3–7]. Still, the primate dopamine system has diverged significantly from that of rodents, exhibiting greatly-expanded and uniquely-distributed cortical and subcortical innervation patterns [8]. Here we bridge the gap between rodent perturbation studies and monkey electrophysiology using chronic electrical microstimulation of macaque VTA (VTA-EM). VTA-EM was found to reinforce cue selection in an operant task and to motivate future cue selection using a Pavlovian paradigm. Moreover, by combining VTA-EM with concurrent functional magnetic resonance imaging (fMRI), we demonstrated that VTA-EM increased fMRI activity throughout most of the dopaminergic reward system. These results establish a causative role for primate VTA in regulating stimulus-specific reinforcement and motivation as well as modulating activity throughout the reward system.

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The cortical areas that process disparity-defined motion-in-depth (i.e., cyclopean stereomotion [CSM]) were characterized with functional magnetic resonance imaging (fMRI) in two awake, behaving macaques. The experimental protocol was similar to previous human neuroimaging studies. We contrasted the responses to dynamic random-dot patterns that continuously changed their binocular disparity over time with those to a control condition that shared the same properties, except that the temporal frames were shuffled. A whole-brain voxel-wise analysis revealed that in all four cortical hemispheres, three areas showed consistent sensitivity to CSM. Two of them were localized respectively in the lower bank of the superior temporal sulcus (CSMSTS) and on the neighboring infero-temporal gyrus (CSMITG). The third area was situated in the posterior parietal cortex (CSMPPC). Additional regions of interest-based analyses within retinotopic areas defined in both animals indicated weaker but significant responses to CSM within the MT cluster (most notably in areas MSTv and FST). Altogether, our results are in agreement with previous findings in both human and macaque and suggest that the cortical areas that process CSM are relatively well preserved between the two primate species.