Modulations of foveal vision associated with microsaccade preparation.

It is known that attention shifts prior to a saccade to start processing the saccade target before it lands in the foveola, the high-resolution region of the retina. Yet, once the target is foveated, microsaccades, tiny saccades maintaining the fixated object within the fovea, continue to occur. What is the link between these eye movements and attention? There is growing evidence that these eye movements are associated with covert shifts of attention in the visual periphery, when the attended stimuli are presented far from the center of gaze. Yet, microsaccades are primarily used to explore complex foveal stimuli and to optimize fine spatial vision in the foveola, suggesting that the influences of microsaccades on attention may predominantly impact vision at this scale. To address this question we tracked gaze position with high precision and briefly presented high-acuity stimuli at predefined foveal locations right before microsaccade execution. Our results show that visual discrimination changes prior to microsaccade onset. An enhancement occurs at the microsaccade target location. This modulation is highly selective and it is coupled with a drastic impairment at the opposite foveal location, just a few arcminutes away. This effect is strongest when stimuli are presented closer to the eye movement onset time. These findings reveal that the link between attention and microsaccades is deeper than previously thought, exerting its strongest effects within the foveola. As a result, during fixation, foveal vision is constantly being reshaped both in space and in time with the occurrence of microsaccades.

Task-driven visual exploration at the foveal scale.

Humans use saccades to inspect objects of interest with the foveola, the small region of the retina with highest acuity. This process of visual exploration is normally studied over large scenes. However, in everyday tasks, the stimulus within the foveola is complex, and the need for visual exploration may extend to this smaller scale. We have previously shown that fixational eye movements, in particular microsaccades, play an important role in fine spatial vision. Here, we investigate whether task-driven visual exploration occurs during the fixation pauses in between large saccades. Observers judged the expression of faces covering approximately 1°, as if viewed from a distance of many meters. We use a custom system for accurately localizing the line of sight and continually track gaze position at high resolution. Our findings reveal that active spatial exploration, a process driven by the goals of the task, takes place at the foveal scale. The scanning strategies used at this scale resemble those used when examining larger scenes, with idiosyncrasies maintained across spatial scales. These findings suggest that the visual system possesses not only a coarser priority map of the extrafoveal space to guide saccades, but also a finer-grained priority map that is used to guide microsaccades once the region of interest is foveated.

Ultra-fine resolution of pre-saccadic attention in the fovea.

Microsaccades, the tiny gaze relocations that occurr during fixation, have been linked to covert attention deployed degrees away from the center of gaze. However, the link between attention and microsaccades is deeper in that it also unfolds at the foveal scale. Here, we have examined the spatial grain of pre-microsaccadic attention across the 1° foveola. Through the use of high-precision eye-tracking and gaze-contingent display system that achieves arcminute precision in gaze localization, we have shown that the spotlight of attention at this scale can reach a strikingly high resolution, in the order of 0.17°. Further, when a microsaccade occurs, vision is modulated in a peculiar way across the foveola; whereas fine spatial vision is enhanced at the microsaccade goal location, it drops at the very center of gaze, where acuity is normally highest. These results reveal the finesse of the visuomotor system and of the interplay between eye movements and attention.

Intracortical microstimulation of human somatosensory cortex is sufficient to induce perceptual biases.

Time-order error, a psychophysical phenomenon in which the duration in between successive stimuli alters perception, has been studied for decades by neuroscientists and psychologists. To date, however, the locus of these effects is unknown. We use intracortical microstimulation of somatosensory cortex in humans as a tool to bypass initial stages of processing and restrict the possible locations that signals could be modified. We find that, using both amplitude discrimination and magnitude estimation paradigms, intracortical microstimulation reliably evoked time-order errors across all participants. Points of subjective equality were symmetrically shifted during amplitude discrimination experiments and the intensity of a successive stimulus was perceived as being more intense when compared to single stimulus trials in magnitude estimation experiments. The error was reduced for both paradigms at longer inter-stimulus intervals. These results show that direct activation of primary somatosensory cortex is sufficient to induce time-order errors.

Microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortex.

The primary motor (M1) and somatosensory (S1) cortices play critical roles in motor control but the signaling between these structures is poorly understood. To fill this gap, we recorded - in three participants in an ongoing human clinical trial (NCT01894802) for people with paralyzed hands - the responses evoked in the hand and arm representations of M1 during intracortical microstimulation (ICMS) in the hand representation of S1. We found that ICMS of S1 activated some M1 neurons at short, fixed latencies consistent with monosynaptic activation. Additionally, most of the ICMS-evoked responses in M1 were more variable in time, suggesting indirect effects of stimulation. The spatial pattern of M1 activation varied systematically: S1 electrodes that elicited percepts in a finger preferentially activated M1 neurons excited during that finger's movement. Moreover, the indirect effects of S1 ICMS on M1 were context dependent, such that the magnitude and even sign relative to baseline varied across tasks. We tested the implications of these effects for brain-control of a virtual hand, in which ICMS conveyed tactile feedback. While ICMS-evoked activation of M1 disrupted decoder performance, this disruption was minimized using biomimetic stimulation, which emphasizes contact transients at the onset and offset of grasp, and reduces sustained stimulation.

Biomimetic multi-channel microstimulation of somatosensory cortex conveys high resolution force feedback for bionic hands.

Manual interactions with objects are supported by tactile signals from the hand. This tactile feedback can be restored in brain-controlled bionic hands via intracortical microstimulation (ICMS) of somatosensory cortex (S1). In ICMS-based tactile feedback, contact force can be signaled by modulating the stimulation intensity based on the output of force sensors on the bionic hand, which in turn modulates the perceived magnitude of the sensation. In the present study, we gauged the dynamic range and precision of ICMS-based force feedback in three human participants implanted with arrays of microelectrodes in S1. To this end, we measured the increases in sensation magnitude resulting from increases in ICMS amplitude and participant's ability to distinguish between different intensity levels. We then assessed whether we could improve the fidelity of this feedback by implementing "biomimetic" ICMS-trains, designed to evoke patterns of neuronal activity that more closely mimic those in natural touch, and by delivering ICMS through multiple channels at once. We found that multi-channel biomimetic ICMS gives rise to stronger and more distinguishable sensations than does its single-channel counterpart. Finally, we implemented biomimetic multi-channel feedback in a bionic hand and had the participant perform a compliance discrimination task. We found that biomimetic multi-channel tactile feedback yielded improved discrimination over its single-channel linear counterpart. We conclude that multi-channel biomimetic ICMS conveys finely graded force feedback that more closely approximates the sensitivity conferred by natural touch.

Tessellation of artificial touch via microstimulation of human somatosensory cortex.

When we interact with objects, we rely on signals from the hand that convey information about the object and our interaction with it. A basic feature of these interactions, the locations of contacts between the hand and object, is often only available via the sense of touch. Information about locations of contact between a brain-controlled bionic hand and an object can be signaled via intracortical microstimulation (ICMS) of somatosensory cortex (S1), which evokes touch sensations that are localized to a specific patch of skin. To provide intuitive location information, tactile sensors on the robotic hand drive ICMS through electrodes that evoke sensations at skin locations matching sensor locations. This approach requires that ICMS-evoked sensations be focal, stable, and distributed over the hand. To systematically investigate the localization of ICMS-evoked sensations, we analyzed the projected fields (PFs) of ICMS-evoked sensations - their location and spatial extent - from reports obtained over multiple years from three participants implanted with microelectrode arrays in S1. First, we found that PFs vary widely in their size across electrodes, are highly stable within electrode, are distributed over large swaths of each participant's hand, and increase in size as the amplitude or frequency of ICMS increases. Second, while PF locations match the locations of the receptive fields (RFs) of the neurons near the stimulating electrode, PFs tend to be subsumed by the corresponding RFs. Third, multi-channel stimulation gives rise to a PF that reflects the conjunction of the PFs of the component channels. By stimulating through electrodes with largely overlapping PFs, then, we can evoke a sensation that is experienced primarily at the intersection of the component PFs. To assess the functional consequence of this phenomenon, we implemented multichannel ICMS-based feedback in a bionic hand and demonstrated that the resulting sensations are more localizable than are those evoked via single-channel ICMS.

Transient perceptual enhancements resulting from selective shifts of exogenous attention in the central fovea.

Exogenous attention, a powerful adaptive tool that quickly and involuntarily orients processing resources to salient stimuli, has traditionally been studied in the lower-resolution parafoveal and peripheral visual field.1-4 It is not known whether and how it operates across the 1° central fovea where visual resolution peaks.5,6 Here we investigated the dynamics of exogenous attention in the foveola. To circumvent the challenges posed by fixational eye movements at this scale, we used high-precision eye-tracking and gaze-contingent display control for retinal stabilization.7 High-acuity stimuli were briefly presented foveally at varying delays following an exogenous cue. Attended and unattended locations were just a few arcminutes away from the preferred locus of fixation. Our results show that for short temporal delays, observers' ability to discriminate fine detail is enhanced at the cued location. This enhancement is highly localized and does not extend to the nearby locations only 16' away. On a longer timescale, instead, we report an inverse effect: paradoxically, acuity is sharper at the unattended locations, resembling the phenomenon of inhibition of return at much larger eccentricities.8-10 Although exogenous attention represents a mechanism for low-cost monitoring of the environment in the extrafoveal space, these findings show that, in the foveola, it transiently modulates vision of detail with a high degree of resolution. Together with inhibition of return, it may aid visual exploration of complex foveal stimuli.11.