Cortical Stimulation Paired With Volitional Unimanual Movement Affects Interhemispheric Communication

Cortical stimulation (CS) of the motor cortex can cause excitability changes in both hemispheres, showing potential to be a technique for clinical rehabilitation of motor function. However, previous studies that have investigated the effects of delivering CS during movement typically focus on a single hemisphere. On the other hand, studies exploring interhemispheric interactions typically deliver CS at rest. We sought to bridge these two approaches by documenting the consequences of delivering CS to a single motor cortex during different phases of contralateral and ipsilateral limb movement, and simultaneously assessing changes in interactions within and between the hemispheres via local field potential (LFP) recordings. Three macaques were trained in a unimanual reaction time (RT) task and implanted with epidural or intracortical electrodes over bilateral motor cortices. During a given session CS was delivered to one hemisphere with respect to movements of either the contralateral or ipsilateral limb. Stimulation delivered before contralateral limb movement onset shortened the contralateral limb RT. In contrast, stimulation delivered after the end of contralateral movement increased contralateral RT but decreased ipsilateral RT. Stimulation delivered before ipsilateral limb movement decreased ipsilateral RT. All other stimulus conditions as well as random stimulation and periodic stimulation did not have consistently significant effects on either limb. Simultaneous LFP recordings from one animal revealed correlations between changes in interhemispheric alpha band coherence and changes in RT, suggesting that alpha activity may be indicative of interhemispheric communication. These results show that changes caused by CS to the functional coupling within and between precentral cortices is contingent on the timing of CS relative to movement.

The Motor Cortex Has Independent Representations for Ipsilateral and Contralateral Arm Movements But Correlated Representations for Grasping

Motor commands for the arm and hand generally arise from the contralateral motor cortex, where most of the relevant corticospinal tract originates. However, the ipsilateral motor cortex shows activity related to arm movement despite the lack of direct connections. The extent to which the activity related to ipsilateral movement is independent from that related to contralateral movement is unclear based on conflicting conclusions in prior work. Here we investigate bilateral arm and hand movement tasks completed by two human subjects with intracortical microelectrode arrays implanted in the left hand and arm area of the motor cortex. Neural activity was recorded while they attempted to perform arm and hand movements in a virtual environment. This enabled us to quantify the strength and independence of motor cortical activity related to continuous movements of each arm. We also investigated the subjects’ ability to control both arms through a brain–computer interface. Through a number of experiments, we found that ipsilateral arm movement was represented independently of, but more weakly than, contralateral arm movement. However, the representation of grasping was correlated between the two hands. This difference between hand and arm representation was unexpected and poses new questions about the different ways the motor cortex controls the hands and arms.

Primary motor cortex has independent representations for ipsilateral and contralateral arm movements but correlated representations for grasping

Motor commands for the arms and hands generally originate in contralateral motor cortex anatomically. However, ipsilateral primary motor cortex shows activity related to arm movement despite the lack of direct connections. The extent to which the activity related to ipsilateral movement is independent from that related to contralateral movement is unclear based on conflicting conclusions in prior work. Here we present the results of bilateral arm and hand movement tasks completed by two human subjects with intracortical microelectrode arrays implanted in left primary motor cortex for a clinical brain-computer interface study. Neural activity was recorded while they attempted to perform arm and hand movements in a virtual environment. This enabled us to quantify the strength and independence of motor cortical activity related to continuous movements of each arm. We also investigated the subjects’ ability to control both arms through a brain-computer interface system. Through a number of experiments, we found that ipsilateral arm movement was represented independently of, but more weakly than, contralateral arm movement. However, the representation of grasping was correlated between the two hands. This difference between hand and arm representation was unexpected, and poses new questions about the different ways primary motor cortex controls hands and arms.

Octopamine stabilizes conduction reliability of an unmyelinated axon during hypoxic stress

Mechanisms that could mitigate the effects of hypoxia on neuronal signaling are incompletely understood. We show that axonal performance of a locust visual interneuron varied depending on oxygen availability. To induce hypoxia, tracheae supplying the thoracic nervous system were surgically lesioned and action potentials in the axon of the descending contralateral movement detector (DCMD) neuron passing through this region were monitored extracellularly. The conduction velocity and fidelity of action potentials decreased throughout a 45-min experiment in hypoxic preparations, whereas conduction reliability remained constant when the tracheae were left intact. The reduction in conduction velocity was exacerbated for action potentials firing at high instantaneous frequencies. Bath application of octopamine mitigated the loss of conduction velocity and fidelity. Action potential conduction was more vulnerable in portions of the axon passing through the mesothoracic ganglion than in the connectives between ganglia, indicating that hypoxic modulation of the extracellular environment of the neuropil has an important role to play. In intact locusts, octopamine and its antagonist, epinastine, had effects on the entry to, and recovery from, anoxic coma consistent with octopamine increasing overall neural performance during hypoxia. These effects could have functional relevance for the animal during periods of environmental or activity-induced hypoxia.

Background complexity affects response of a looming-sensitive neuron to object motion

An increasing number of studies show how stimulus complexity affects the responses of looming-sensitive neurons across multiple animal taxa. Locusts contain a well-described, descending motion-sensitive pathway that is preferentially looming sensitive. However, the lobula giant movement detector/descending contralateral movement detector (LGMD/DCMD) pathway responds to more than simple objects approaching at constant, predictable trajectories. In this study, we presented Locusta migratoria with a series of complex three-dimensional visual stimuli presented while simultaneously recording DCMD activity extracellularly. In addition to a frontal looming stimulus, we used a combination of compound trajectories (nonlooming transitioning to looming) presented at different velocities and onto a simple, scattered, or progressive flow field background. Regardless of stimulus background, DCMD responses to looming were characteristic and related to previously described effects of azimuthal approach angle and velocity of object expansion. However, increasing background complexity caused reduced firing rates, delayed peaks, shorter rise phases, and longer fall phases. DCMD responded to transitions to looming with a characteristic drop in a firing rate that was relatively invariant across most stimulus combinations and occurred regardless of stimulus background. Spike numbers were higher in the presence of the scattered background and reduced in the flow field background. We show that DCMD response time to a transition depends on unique expansion parameters of the moving stimulus irrespective of background complexity. Our results show how background complexity shapes DCMD responses to looming stimuli, which is explained within a behavioral context.

Spatiotemporal stimulus properties modulate responses to trajectory changes in a locust looming-sensitive pathway

The lobula giant movement detector (LGMD) and descending contralateral movement detector (DCMD) constitute one motion-sensitive pathway in the locust visual system that is implicated in collision-avoidance behaviors. While this pathway is thought to respond preferentially to objects approaching on a direct collision course, emerging studies suggest the firing rate is able to monitor more complicated movements that would occur under natural conditions. While previous studies have compared the response of the DCMD to objects on collision courses that travel at different speeds, velocity has not been manipulated for other simple or compound trajectories. Here we test the possibility that the LGMD/DCMD pathway is capable of responding uniquely to complex aspects of object motion, including translation and trajectory changes at different velocities. We found that the response of the DCMD to translational motion initiated in the caudal visual field was a low-amplitude peak in firing rate that occurred before the object crossed 90° azimuth that was invariant to different object velocities. Direct looms at different velocities resulted in peak firing rates that occurred later in time and with greater amplitude for higher velocities. In response to transitions from translational motion to a collision course, the firing rate change depended on both the location within the visual field and the velocity. These results suggest that this pathway is capable of conveying information about multiple properties of a moving object's trajectory.

Motion dazzle: a locust's eye view

Motion dazzle describes high-contrast patterns (e.g. zigzags on snakes and dazzle paint on World War I ships) that do not conceal an object, but inhibit an observer's perception of its motion. However, there is limited evidence for this phenomenon. Locusts have a pair of descending contralateral movement detector (DCMD) neurons which respond to predator-like looming objects and trigger escape responses. Within the network providing input to a DCMD, separate channels are excited when moving edges cause areas of the visual field to brighten or darken, respectively, and these stimuli interact antagonistically. When a looming square has an upper half and lower half that are both darker than background, it elicits a stronger DCMD response than the upper half does alone. However, when a looming square has a darker-than-background upper half and a brighter-than-background lower half, it elicits a weaker DCMD response than its upper half does alone. This effect allows high-contrast patterns to weaken and delay DCMD response parameters implicated in escape decisions, and is analogous to motion dazzle. However, the motion dazzle effect does not provide the best means of motion camouflage, because uniform bright squares, or low-contrast squares, elicit weaker DCMD responses than high-contrast, half dark, half bright squares.

A looming-sensitive pathway responds to changes in the trajectory of object motion

Two identified locust neurons, the lobula giant movement detector (LGMD) and its postsynaptic partner, the descending contralateral movement detector (DCMD), constitute one motion-sensitive pathway in the visual system that responds preferentially to objects that approach on a direct collision course and are implicated in collision-avoidance behavior. Previously described responses to the approach of paired objects and approaches at different time intervals (Guest BB, Gray JR. J Neurophysiol 95: 1428–1441, 2006) suggest that this pathway may also be affected by more complicated movements in the locust's visual environment. To test this possibility we presented stationary locusts with disks traveling along combinations of colliding (looming), noncolliding (translatory), and near-miss trajectories. Distinctly different responses to different trajectories and trajectory changes demonstrate that DCMD responds to complex aspects of local visual motion. DCMD peak firing rates associated with the time of collision remained relatively invariant after a trajectory change from translation to looming. Translatory motion initiated in the frontal visual field generated a larger peak firing rate relative to object motion initiated in the posterior visual field, and the peak varied with simulated distance from the eye. Transition from translation to looming produced a transient decrease in the firing rate, whereas transition away from looming produced a transient increase. The change in firing rate at the time of transition was strongly correlated with unique expansion parameters described by the instantaneous angular acceleration of the leading edge and subtense angle of the disk. However, response time remained invariant. While these results may reflect low spatial resolution of the compound eye, they also suggest that this motion-sensitive pathway may be capable of monitoring dynamic expansion properties of objects that change the trajectory of motion.

Arousal Facilitates Collision Avoidance Mediated by a Looming Sensitive Visual Neuron in a Flying Locust

Locusts have two large collision-detecting neurons, the descending contralateral movement detectors (DCMDs) that signal object approach and trigger evasive glides during flight. We sought to investigate whether vision for action, when the locust is in an aroused state rather than a passive viewer, significantly alters visual processing in this collision-detecting pathway. To do this we used two different approaches to determine how the arousal state of a locust affects the prolonged periods of high-frequency spikes typical of the DCMD response to approaching objects that trigger evasive glides. First, we manipulated arousal state in the locust by applying a brief mechanical stimulation to the hind leg; this type of change of state occurs when gregarious locusts accumulate in high-density swarms. Second, we examined DCMD responses during flight because flight produces a heightened physiological state of arousal in locusts. When arousal was induced by either method we found that the DCMD response recovered from a previously habituated state; that it followed object motion throughout approach; and—most important—that it was significantly more likely to generate the maintained spike frequencies capable of evoking gliding dives even with extremely short intervals (1.8 s) between approaches. Overall, tethered flying locusts responded to 41% of simulated approaching objects (sets of 6 with 1.8 s ISI). When we injected epinastine, the neuronal octopamine receptor antagonist, into the hemolymph responsiveness declined to 12%, suggesting that octopamine plays a significant role in maintaining responsiveness of the DCMD and the locust to visual stimuli during flight.