Exploring the role of the substantia nigra pars reticulata in eye movements.

Experiments that demonstrated a role for the substantia nigra in eye movements have played an important role in our understanding of the function of the basal ganglia in behavior more broadly. In this review we explore more recent experiments that extend the role of the substantia nigra pars reticulata from a simple gate for eye movements to include a role in cognitive processes for eye movements. We review recent evidence suggesting that basal ganglia nuclei beyond the substantia nigra may also play a role in eye movements and the cognitive events leading up to the production of eye movements. We close by pointing out some unresolved questions in our understanding of the relationship of basal ganglia nuclei and eye movements.

Activity in descending dopaminergic neurons represents but is not required for leg movements in the fruit fly Drosophila.

Modulatory descending neurons (DNs) that link the brain to body motor circuits, including dopaminergic DNs (DA-DNs), are thought to contribute to the flexible control of behavior. Dopamine elicits locomotor-like outputs and influences neuronal excitability in isolated body motor circuits over tens of seconds to minutes, but it remains unknown how and over what time scale DA-DN activity relates to movement in behaving animals. To address this question, we identified DA-DNs in the Drosophila brain and developed an electrophysiological preparation to record and manipulate the activity of these cells during behavior. We find that DA-DN spike rates are rapidly modulated during a subset of leg movements and scale with the total speed of ongoing leg movements, whether occurring spontaneously or in response to stimuli. However, activating DA-DNs does not elicit leg movements in intact flies, nor do acute bidirectional manipulations of DA-DN activity affect the probability or speed of leg movements over a time scale of seconds to minutes. Our findings indicate that in the context of intact descending control, changes in DA-DN activity are not sufficient to influence ongoing leg movements and open the door to studies investigating how these cells interact with other descending and local neuromodulatory inputs to influence body motor output.

Locomotor head movements and semicircular canal morphology in primates.

Animal locomotion causes head rotations, which are detected by the semicircular canals of the inner ear. Morphologic features of the canals influence rotational sensitivity, and so it is hypothesized that locomotion and canal morphology are functionally related. Most prior research has compared subjective assessments of animal "agility" with a single determinant of rotational sensitivity: the mean canal radius of curvature (R). In fact, the paired variables of R and body mass are correlated with agility and have been used to infer locomotion in extinct species. To refine models of canal functional morphology and to improve locomotor inferences for extinct species, we compare 3D vector measurements of head rotation during locomotion with 3D vector measures of canal sensitivity. Contrary to the predictions of conventional models that are based upon R, we find that axes of rapid head rotation are not aligned with axes of either high or low sensitivity. Instead, animals with fast head rotations have similar sensitivities in all directions, which they achieve by orienting the three canals of each ear orthogonally (i.e., along planes at 90° angles to one another). The extent to which the canal configuration approaches orthogonality is correlated with rotational head speed independent of body mass and phylogeny, whereas R is not.

A pathway in primate brain for internal monitoring of movements.

It is essential to keep track of the movements we make, and one way to do that is to monitor correlates, or corollary discharges, of neuronal movement commands. We hypothesized that a previously identified pathway from brainstem to frontal cortex might carry corollary discharge signals. We found that neuronal activity in this pathway encodes upcoming eye movements and that inactivating the pathway impairs sequential eye movements consistent with loss of corollary discharge without affecting single eye movements. These results identify a pathway in the brain of the primate Macaca mulatta that conveys corollary discharge signals.

Grabbing Your Attention: The Impact of Finding a First Target in Multiple-Target Search

For over 50 years, the Satisfaction of Search effect, and more recently known as the Subsequent Search Miss (SSM) effect, has plagued the field of radiology. Defined as a decrease in additional target accuracy after detecting a prior target in a visual search, SSM errors are known to underlie both real-world search errors (e.g., a radiologist is more likely to miss a tumor if a different tumor was previously detected) and more simplified, lab-based search errors (e.g., an observer is more likely to miss a target ‘T’ if a different target ‘T’ was previously detected). Unfortunately, little was known about this phenomenon’s cognitive underpinnings and SSM errors have proven difficult to eliminate. However, more recently, experimental research has provided evidence for three different theories of SSM errors: the Satisfaction account, the Perceptual Set account, and the Resource Depletion account. A series of studies examined performance in a multiple-target visual search and aimed to provide support for the Resource Depletion account—a first target consumes cognitive resources leaving less available to process additional targets.

To assess a potential mechanism underlying SSM errors, eye movements were recorded in a multiple-target visual search and were used to explore whether a first target may result in an immediate decrease in second-target accuracy, which is known as an attentional blink. To determine whether other known attentional distractions amplified the effects of finding a first target has on second-target detection, distractors within the immediate vicinity of the targets (i.e., clutter) were measured and compared to accuracy for a second target. To better understand which characteristics of attention were impacted by detecting a first target, individual differences within four characteristics of attention were compared to second-target misses in a multiple-target visual search.

The results demonstrated that an attentional blink underlies SSM errors with a decrease in second-target accuracy from 135ms-405ms after detection or re-fixating a first target. The effects of clutter were exacerbated after finding a first target causing a greater decrease in second-target accuracy as clutter increased around a second-target. The attentional characteristics of modulation and vigilance were correlated with second- target misses and suggest that worse attentional modulation and vigilance are predictive of more second-target misses. Taken together, these result are used as the foundation to support a new theory of SSM errors, the Flux Capacitor theory. The Flux Capacitor theory predicts that once a target is found, it is maintained as an attentional template in working memory, which consumes attentional resources that could otherwise be used to detect additional targets. This theory not only proposes why attentional resources are consumed by a first target, but encompasses the research in support of all three SSM theories in an effort to establish a grand, unified theory of SSM errors.

Descending Control of Limb Movements in Drosophila melanogaster

Because the interactions between feedforward influences are inextricably linked during many motor outputs (including but not limited to walking), the contribution of descending inputs to the generation of movements is difficult to study. Here we take advantage of the relatively small number of descending neurons (DNs) in the Drosophila melanogaster model system. We first characterize the number and distribution of the DN populations, then present a novel load free preparation, which enables the study of descending control on limb movements in a context where sensory feedback can be is reduced while leaving the nervous system, musculature, and cuticle of the animal relatively intact. Lastly we use in-vivo whole cell patch clamp electrophysiology to characterize the role of individual DNs in response to specific sensory stimuli and in relationship to movement. We find that there are approximately 1100 DNs in Drosophila that are distributed across six clusters. Input from these DNs is not necessary for coordinated motor activity, which can be generated by the thoracic ganglion, but is necessary for the specific combinations of joint movements typically observed in walking. Lastly, we identify a particular cluster of DNs that are tuned to sensory stimuli and innervate the leg neuromeres. We propose that a multi-layered interaction between these DNs, other DNs, and motor circuits in the thoracic ganglia enable the diverse but well-coordinated range of motor outputs an animal might exhibit.