Brian D. Corneil

Cognitive control signals for neural prosthetics

Recent development of neural prosthetics for assisting paralyzed patients has focused on decoding intended hand trajectories from motor cortical neurons and using this signal to control external devices. In this study, higher level signals related to the goals of movements were decoded from three monkeys and used to position cursors on a computer screen without the animals emitting any behavior. Their performance in this task improved over a period of weeks. Expected value signals related to fluid preference, the expected magnitude, or probability of reward were decoded simultaneously with the intended goal. For neural prosthetic applications, the goal signals can be used to operate computers, robots, and vehicles, whereas the expected value signals can be used to continuously monitor a paralyzed patients preferences and motivation.

Combined eye-head gaze shifts to visual and auditory targets in humans.

We studied the characteristics of combined eye-head gaze shifts in human subjects to determine whether they used similar strategies when looking at visual (V), auditory (A), and combined (V+A) targets located at several target eccentricities along the horizontal meridian. Subjects displayed considerable variability in the combinations of eye and head movement used to orient to the targets, ranging from those who always aligned their head close to the target, to those who relied predominantly on eye movements and only moved their head when the target was located beyond the limits of ocular motility. For a given subject, there was almost no variability in the amount of eye and head movement in the three target conditions (V, A, V+A). The time to initiate a gaze shift was influenced by stimulus modality and eccentricity. Auditory targets produced the longest latencies when located centrally (less than 20° eccentricity), whereas visual targets evoked the longest latencies when located peripherally (greater than 40° eccentricity). Combined targets (V+A) elicited the shortest latency reaction times at all eccentricities. The peak velocity of gaze shifts was also affected by target modality. At eccentricities between 10 and 30°, peak gaze velocity was greater for movements to visual targets than for movements to auditory targets. Movements to the combined target were of comparable speed with movements to visual targets. Despite the modality-specific differences in reaction latency and peak gaze velocity, the consistency of combinations of eye and head movement within subjects suggests that visual and auditory signals are remapped into a common reference frame for controlling orienting gaze shifts. A likely candidate is the deeper layers of the superior colliculus, because visual and auditory signals converge directly onto the neurons projecting to the eye and head premotor centers.

Visual Responses on Neck Muscles Reveal Selective Gating that Prevents Express Saccades

Express saccades promote the acquisition of visual targets at extremely short reaction times. Because of the heads considerable inertia, it is unknown whether express saccades are accompanied by a parallel command to the head. Here, by recording electromyographic (EMG) activity from monkey neck muscles, we demonstrate that visual target presentation elicits time-locked, lateralized recruitment of neck muscles at extremely short latencies (55-95 ms). Remarkably, such recruitment not only accompanies express saccades, but also precedes nonexpress saccades, occasionally by up to 150 ms. These results demonstrate selective gating of components of descending commands from the superior colliculus to prevent express saccades yet permit recruitment of a head orienting synergy. We conclude that such selective gating aids eye-head coordination by permitting force development at neck muscles while a decision to commit to a gaze shift is being made, optimizing the contribution of the more inertial head to the ensuing gaze shift.

Evidence for interactions between target selection and visual fixation for saccade generation in humans.

We examined the processes controlling selective orientation, specifically the processes required for generating saccadic eye movements in humans. Before a saccadic eye movement can be initiated, active visual fixation must be disengaged from the current point of fixation and a new target selected. We investigated whether these neural processes occur independently or interactively by devising a simple, multimodal choice reaction task in which subjects were asked to direct their gaze away from a central visual fixation target to an eccentric visual target while ignoring a simultaneous auditory distractor. Subjects had more difficulty suppressing incorrect movements toward the distractor when the fixation target was extinguished prior to onset of the eccentric target than when the fixation target remained illuminated during eccentric target presentation. Subjects with the shortest saccadic reaction times produced the most incorrect movements. These results support a recent hypothesis suggesting that the processes of disengaging active visual fixation and selecting a new saccade target are interrelated and arise, at least in part, from a change of activity within the superior colliculus.

Neuromuscular consequences of reflexive covert orienting

Visual stimulus presentation activates the oculomotor network without requiring a gaze shift. Here, we demonstrate that primate neck muscles are recruited during such reflexive covert orienting in a manner that parallels activity recorded from the superior colliculus (SC). Our results indicate the presence of a brainstem circuit whereby reflexive covert orienting is prevented from shifting gaze, but recruits neck muscles, predicting that similarities between SC and neck muscle activity should extend to other cognitive processes that are known to influence SC activity.

Overt Responses during Covert Orienting

A distributed network of cortical and subcortical brain areas controls our oculomotor behavior. This network includes the superior colliculus (SC), which coordinates an ancient visual grasp reflex via outputs that ramify widely within the brainstem and spinal cord, accessing saccadic and other premotor and autonomic circuits. In this Review, we discuss recent results correlating subliminal SC activity in the absence of saccades with diverse components of the visual grasp reflex, including neck and limb muscle recruitment, pupil dilation, and microsaccade propensity. Such subtle manifestations of covert orienting are accessible in the motor periphery and may provide the next generation of oculomotor biomarkers in health and disease.

Engagement of visual fixation suppresses sensory responsiveness and multisensory integration in the primate superior colliculus

Neurons in the intermediate and deep layers of the superior colliculus (SC) often exhibit sensory‐related activity in addition to discharging for saccadic eye movements. These two patterns of activity can combine so that modifications of the sensory response can lead to changes in orienting behaviour. Can behavioural factors, however, influence sensory activity? In this study of rhesus monkeys, we isolate one behavioural factor, the state of visual fixation, and examine its influences on sensory processing and multisensory integration in the primate SC. Two interleaved fixation conditions were used: a FIX condition requiring exogenous fixation of a visible fixation point; and a FIX‐BLINK condition, requiring endogenous fixation in the absence of a visible fixation point. Neurons of the SC were influenced by fixation state, exhibiting both lower levels of sensory activity and reduced multisensory interactions when fixation was exogenously engaged on a visible fixation point. These results are consistent with active visual fixation suppressing responses to extraneous stimuli, and thus demonstrate that sensory processing and multisensory responses in the SC are not dependent solely on the physical properties of the sensory environment, but are also dynamically influenced by the behavioural state of the animal.

Marked non-uniformity of fiber-type composition in the primate suboccipital muscle obliquus capitis inferior

Abstract Obliquus capitis inferior (OCI) is a monoarticular suboccipital muscle linking the transverse process of the atlas (C1) to the spinous process of the axis (C2). Histochemical analysis of fiber-type composition showed that the muscle has a marked gradient of fiber-type distribution in which type I fibers comprise 95–100% of fibers in the deepest region but less than 10% of fibers in the superficial layer. Step-like changes in fiber-type proportions occurred between groups of fascicles. In most instances the boundaries between these fascicles did not exhibit different perimysial features from those fascicles with similar fiber-type proportions. OCI contained large numbers of muscle spindles, which were concentrated in deep regions rich in type I fibers. The degree of nonuniformity in fiber-type distribution seen in OCI is unusually large when compared with patterns described in other primate muscles, and has implications for the way that the muscle is studied anatomically and physiologically.

Recruitment of a Head-Turning Synergy by Low-Frequency Activity in the Primate Superior Colliculus

Low-frequency activity within the oculomotor system helps bridge sensation and action. Given ocular stability, low-frequency activity sustained by some neurons within the intermediate and deep superior colliculus (dSC) is assumed to be separated from motor output. However, the dSC is an orienting structure and the influence of low-frequency dSC activity at other effectors remains untested. We studied this by simultaneously recording activity from saccade-related dSC neurons and electromyographic (EMG) activity from neck muscles that turn the head. Monkeys performed a gap-saccade paradigm with varying levels of reward expectancy. Despite head restraint and even for relatively small target eccentricities (<or=10 degrees ), increasing reward expectancy for a given target increased the level of low-frequency activity on dSC neurons encoding saccades to the rewarded target and increased the recruitment of a neck muscle synergy that would turn the head toward the target. The magnitude of neck muscle recruitment correlated positively on a trial-by-trial basis with the level of low-frequency dSC activity, and such correlations were optimized when neck muscle activity was shifted about 20 ms later to account for delays in the tecto-reticulo-spinal pathway. Further, dSC activity discriminated about the side of target presentation approximately 11 ms earlier than neck EMG activity. Considered alongside neck EMG responses evoked causally by SC stimulation, our results are consistent with low-frequency dSC activity recruiting a head-turning synergy. Our results support a brain stem circuit wherein the magnitude of neck muscle recruitment reflects the difference in comparative low-frequency activation across both dSCs, perhaps because of mutually inhibitory interactions within downstream head premotor circuits.

Magnetic resonance image-guided implantation of chronic recording electrodes in the macaque intraparietal sulcus

The implantation of chronic recording electrodes in the brain has been shown to be a valuable method for simultaneously recording from many neurons. However, precise placement of these electrodes, crucial for successful recording, is challenging if the target area is not on the brain surface. Here we present a stereotaxic implantation procedure to chronically implant bundles of recording electrodes into macaque cortical sulci, employing magnetic resonance (MR) imaging to determine stereotaxic coordinates of target location and sulcus orientation. Using this method in four animals, we recorded simultaneously the spiking activity and the local field potential from the parietal reach region (PRR), located in the medial bank of the intraparietal sulcus (IPS), while the animal performed a reach movement task. Fifty percent of all electrodes recorded spiking activity during the first 2 post-operative months, indicating their placement within cortical gray matter. Chronic neural activity was similar to standard single electrode recordings in PRR, as reported previously. These results indicate that this MR image-guided implantation technique can provide sufficient placement accuracy in cortical sulci and subcortical structures. Moreover, this technique may be useful for future cortical prosthesis applications in humans that require implants within sulci.