Gaze-Related Activity in Primate Frontal Cortex Predicts and Mitigates Spatial Uncertainty

A remarkable feature of primate behavior is the ability to predict future events based on past experience and current sensory cues. To understand how the brain plans movements in the presence of unstable cues, we recorded gaze-related activity in the frontal cortex of two monkeys engaged in a quasi-predictable cue-conflict task. Animals were trained to look toward remembered visual targets in the presence of a landmark that shifted with fixed amplitude but randomized direction. As simulated by a probabilistic model based on known physiology/behavior, gaze end points assumed a circular distribution around the target, mirroring the possible directions of the landmark shift. This predictive strategy was reflected in frontal cortex activity (especially supplementary eye fields), which anticipated future gaze distributions before the actual landmark shift. In general, these results implicate prefrontal cortex in the predictive integration of environmental cues and their learned statistical properties to mitigate spatial uncertainty.

Spatiotemporal coding in the macaque supplementary eye fields: landmark influence in the target-to-gaze transformation

ABSTRACTEye-centered (egocentric) and landmark-centered (allocentric) visual signals influence spatial cognition, navigation and goal-directed action, but the neural mechanisms that integrate these signals for motor control are poorly understood. A likely candidate for ego / allocentric integration in the gaze control system is the supplementary eye fields (SEF), a mediofrontal structure with high-level ‘executive’ functions, spatially tuned visual / motor response fields, and reciprocal projections with the frontal eye fields (FEF). To test this hypothesis, we trained two head-unrestrained animals to saccade toward a remembered visual target in the presence of a visual landmark that shifted during the delay, causing gaze end points to shift partially in the same direction. 256 SEF neurons were recorded, including 68 with spatially tuned response fields. Model fits to the latter established that, like the FEF and superior colliculus, spatially tuned SEF responses primarily showed an egocentric (eye-centered) target-to-gaze position transformation. However, the landmark shift influenced this default egocentric transformation: during the delay, motor neurons (with no visual response) showed a transient but unintegrated shift (i.e., not correlated with the target-to-gaze transformation), whereas during the saccade-related burst visuomotor neurons showed an integrated shift (i.e., correlated with the target-to-gaze transformation). This differed from our simultaneous FEF recordings (Bharmauria et al., 2020), which showed a transient shift in visuomotor neurons, followed by an integrated response in all motor responses. Based on these findings and past literature, we propose that prefrontal cortex incorporates landmark-centered information into a distributed, eye-centered target-to-gaze transformation through a reciprocal prefrontal circuit.

Stopping smooth pursuit

If a visual object of interest suddenly starts to move, we will try to follow it with a smooth movement of the eyes. This smooth pursuit response aims to reduce image motion on the retina that could blur visual perception. In recent years, our knowledge of the neural control of smooth pursuit initiation has sharply increased. However, stopping smooth pursuit eye movements is less well understood and will be discussed in this paper. The most straightforward way to study smooth pursuit stopping is by interrupting image motion on the retina. This causes eye velocity to decay exponentially towards zero. However, smooth pursuit stopping is not a passive response, as shown by behavioural and electrophysiological evidence. Moreover, smooth pursuit stopping is particularly influenced by active prediction of the upcoming end of the target. Here, we suggest that a particular class of inhibitory neurons of the brainstem, the omnipause neurons, could play a central role in pursuit stopping. Furthermore, the role of supplementary eye fields of the frontal cortex in smooth pursuit stopping is also discussed. This article is part of the themed issue ‘Movement suppression: brain mechanisms for stopping and stillness’.

Recruitment of a contralateral head turning synergy by stimulation of monkey supplementary eye fields

The supplementary eye fields (SEF) are thought to enable higher-level aspects of oculomotor control. The goal of the present experiment was to learn more about the SEF's role in orienting, specifically by examining neck muscle recruitment evoked by stimulation of the SEF. Neck muscle activity was recorded from multiple muscles in two monkeys during SEF stimulation (100 μA, 150–300 ms, 300 Hz, with the head restrained or unrestrained) delivered 200 ms into a gap period, before a visually guided saccade initiated from a central position (doing so avoids confounds between initial position and prestimulation neck muscle activity). SEF stimulation occasionally evoked overt gaze shifts and/or head movements but almost always evoked a response that invariably consisted of a contralateral head turning synergy by increasing activity on contralateral turning muscles and decreasing activity on ipsilateral turning muscles (when background activity was present). Neck muscle responses began well in advance of evoked gaze shifts (∼30 ms after stimulation onset, leading gaze shifts by ∼40–70 ms on average), started earlier and attained a larger magnitude when accompanied by progressively larger gaze shifts, and persisted on trials without overt gaze shifts. The patterns of evoked neck muscle responses resembled those evoked by frontal eye field (FEF) stimulation, except that response latencies from the SEF were ∼10 ms longer. This basic description of the cephalomotor command evoked by SEF stimulation suggests that this structure, while further removed from the motor periphery than the FEF, accesses premotor orienting circuits in the brain stem and spinal cord in a similar manner.

The Neural Basis of Parallel Saccade Programming: An fMRI Study

The neural basis of parallel saccade programming was examined in an event-related fMRI study using a variation of the double-step saccade paradigm. Two double-step conditions were used: one enabled the second saccade to be partially programmed in parallel with the first saccade while in a second condition both saccades had to be prepared serially. The intersaccadic interval, observed in the parallel programming (PP) condition, was significantly reduced compared with latency in the serial programming (SP) condition and also to the latency of single saccades in control conditions. The fMRI analysis revealed greater activity (BOLD response) in the frontal and parietal eye fields for the PP condition compared with the SP double-step condition and when compared with the single-saccade control conditions. By contrast, activity in the supplementary eye fields was greater for the double-step condition than the single-step condition but did not distinguish between the PP and SP requirements. The role of the frontal eye fields in PP may be related to the advanced temporal preparation and increased salience of the second saccade goal that may mediate activity in other downstream structures, such as the superior colliculus. The parietal lobes may be involved in the preparation for spatial remapping, which is required in double-step conditions. The supplementary eye fields appear to have a more general role in planning saccade sequences that may be related to error monitoring and the control over the execution of the correct sequence of responses.