Mapping the Macaque Superior Temporal Sulcus: Functional Delineation of Vergence and Version Eye-Movement-Related Activity

Abstract

It is currently thought that the primate oculomotor system has evolved distinct but interrelated subsystems to generate different types of visually guided eye movements (e.g., saccades/smooth pursuit/vergence). Although progress has been made in elucidating the neural basis of these movement types, no study to date has investigated all three movement types on a large scale and within the same animals. Here, we used fMRI in rhesus macaque monkeys to map the superior temporal sulcus (STS) for BOLD modulation associated with visually guided eye movements. Further, we ascertained whether modulation in a given area was movement type specific and, if not, the modulation each movement type elicited relative to the others (i.e., dominance). Our results show that multiple areas within STS modulate during all movement types studied, including the middle temporal, medial superior temporal, fundus of the superior temporal, lower superior temporal, and dorsal posterior inferotemporal areas. Our results also reveal an area in dorsomedial STS that is modulated almost exclusively by vergence movements. In contrast, we found that ventrolateral STS is driven preferentially during versional movements. These results illuminate an STS network involved in processes associated with multiple eye movement types, illustrate unique patterns of modulation within said network as a function of movement type, and provide evidence for a vergence-specific area within dorsomedial STS. We conclude that producing categorically different eye movement types requires access to a common STS network and that individual network nodes are recruited differentially based upon the type of movement generated.

Midbrain activity supports high-level visual properties in primate temporal cortex

“…By combining fMRI with and without SC inactivation, we found that the same fSTS region exhibited the largest reduction in attention-related BOLD modulation during the attention deficits caused by SC inactivation (figure 1d; 8 ). Relatively little is known about this cortical fSTS region 9-14 and it is unclear why it emerged in fMRI as the primary cortical area dependent on SC activity during the attention task. Our next step was to target this region for extracellular recording (figure 1e) to identify the signals conveyed by neurons and how these signals might depend on superior colliculus activity.…”

Stereomotion processing in the non-human primate brain

“…Finally, we used the detected saccades as regressors of non-interest in our GLM. It is also worth noting that the activations we observed when contrasting our two conditions of interest (CSM vs. TS) are different from the vergence networks as investigated in terms of vergence tracking and vergence steps by Ward and collaborators (Ward et al 2015). Additional analyses based on fixation performances and variance of eye position along the x and y axes during the CSM and TS conditions further demonstrated that eye movements did not impact our results (see supplementary figure 2 and the accompanying text).…”

Three-Dimensional Binocular Eye-Hand Coordination in Normal Vision and with Simulated Visual Impairment

“…Note that with increasing blur levels the contrast of the stimuli decreased. The blur levels employed can be equated to contrast levels of [100,95,78,59,48,35,20] In the binocular blur trials, the stimuli presented to both eyes were blurred. In the monocular blur trials, only the stimuli shown to the left eye were blurred, whereas a sharply focused stimulus was always shown to the right eye.…”

“…The cerebellum, which is directly involved in the control of both pursuit [103,92] and vergence [27,26] eye movements, likely plays an important role in the synchronization of the oculomotor and arm motor systems [61,62]. If the same synchronization signals from the cerebellum were to converge onto separate vergence and pursuit-specific neural loci [25,100], these signals might differentially impact oculomotor tracking performance in depth and along the frontal plane.…”

“…Furthermore, because humans have binocular overlapping visual fields, to inspect objects at different distances or to track objects moving in depth the oculomotor system also executes vergence eye movements, which are unequal slow rotations of each eye that shift the binocular gaze point in depth [15]. Smooth pursuit and vergence eye movements have different tracking characteristics [81] and rely on separate neural substrates [25,100], however, they are similarly encoded in the Frontal Eye Fields region of frontal cortex [24,1].…”