A. K. Moschovakis

The Superior Colliculus : New Approaches for Studying Sensorimotor Integration

Presenting information amassed from more than 30 years of research, this book gathers together the most important pieces of evidence regarding the structure and function of the superior colliculus. It explores the involvement of the superior colliculus in the control of gaze shift and rapid eye movements and provides a detailed discussion of structural features as they relate to functional properties. Placing empirical data in the context of theory, the editors use computational models of the superior colliculus as scaffolds around which to organize psychophysical, neurological, anatomical, and physiological findings concerning its involvement in orienting movements.

Oculomotor areas of the primate frontal lobes: a transneuronal transfer of rabies virus and [14C]-2-deoxyglucose functional imaging study.

We used the [14C]-2-deoxyglucose method to study the location and extent of primate frontal lobe areas activated for saccades and fixation and the retrograde transneuronal transfer of rabies virus to determine whether these regions are oligosynaptically connected with extraocular motoneurons. Fixation-related increases of local cerebral glucose utilization (LCGU) values were found around the fundus of the inferior limb of the arcuate sulcus (AS) just ventral to its genu, in the dorsomedial frontal cortex (DMFC), cingulate cortex, and orbitofrontal cortex. Significant increases of LCGU values were found in and around both banks of the AS, DMFC, and caudal principal, cingulate, and orbitofrontal cortices of monkeys executing visually guided saccades. All of these areas are oligosynaptically connected to extraocular motoneurons, as shown by the presence of retrogradely transneuronally labeled cells after injection of rabies virus in the lateral rectus muscle. Our data demonstrate that the arcuate oculomotor cortex occupies a region considerably larger than the classic, electrical stimulation-defined, frontal eye field. Besides a large part of the anterior bank of the AS, it includes the caudal prearcuate convexity and part of the premotor cortex in the posterior bank of the AS. They also demonstrate that the oculomotor DMFC occupies a small area straddling the ridge of the brain medial to the superior ramus of the AS. Our results support the notion that a network of several interconnected frontal lobe regions is activated during rapid, visually guided eye movements and that their output is conveyed in parallel to subcortical structures projecting to extraocular motoneurons.

Density gradients of trans-synaptically labeled collicular neurons after injections of rabies virus in the lateral rectus muscle of the rhesus monkey.

We evaluated the two‐dimensional distribution of superior colliculus (SC) neurons visualized after retrograde transneuronal transport of rabies virus injected into the lateral rectus muscle of rhesus monkeys to test whether the density of projection neurons might play a role in the spatiotemporal transformation and vector decomposition. If this were the case, the number of horizontal eye movement‐related SC neurons should increase with their distance from the rostral pole of the SC and decrease with their distance from the representation of the horizontal meridian. Labeled neurons of the intermediate SC layers were counted inside a 1‐mm‐wide band that matched the horizontal meridian of the collicular motor map. Local areal densities were plotted against distance from the rostral SC pole. At 2.5 days after inoculation, there was no labeling in the SC. At 3 days, moderate labeling appeared on both sides, mostly in the intermediate layers. At 3.5 days, cell numbers substantially increased and the laminar distribution changed as cells appeared in the superficial SC layers. At 3 days, rostrocaudal density profiles were unimodal, with peaks at locations near 50 degrees (contralateral SC) and 25–30 degrees (ipsilateral SC) horizontal eccentricity. At 3.5 days, distributions were bimodal due to the appearance of a second high‐density region near the rostral pole of the SC. The distribution of SC neurons influencing the abducens nucleus, thus, was nonuniform. Caudal sites contained more neurons, but the experimentally observed density gradients were shallower than the theoretically predicted ones that would be necessary to fully account for the spatiotemporal transformation. Similarly, we studied the distributions of cell densities in the intermediate SC layers along an isoamplitude line (representing saccades of equal amplitudes but different directions). Consistent with theoretical estimates of the density gradients required for vector decomposition, we found that the concentrations of labeled cells were highest in the vicinity of the horizontal meridian but their decrease toward the periphery of the motor map was steeper than predicted. We conclude that SC cell density gradients cannot fully account for the spatiotemporal transformation and vector decomposition in the absence of an additional mechanism such as the previously demonstrated (Grantyn et al., [ 1997 ] Soc. Neurosci. Abstr. 23:1295; Moschovakis et al., [ 1998 ] J. Neurosci. 18:10219–10229) locus‐dependent weighting of the strength of efferent projections to the saccade generators. J. Comp. Neurol. 451:346–361, 2002.

Control of orienting movements: role of multiple tectal projections to the lower brainstem

In movement neuroscience this past decade, a conceptual approach that puts emphasis on population coding was clearly dominant. The purpose of numerous studies has been to define presumably homogeneous groups of neurons on the basis of the correlation of their discharges with sensory and motor events. The goal of this chapter is to stress the importance of taking into account individual properties of neurons, this being an essential prerequisite for a biologically meaningful definition of neuron populations. Taking as an example the executive limb of the neural network controlling gaze movements, we demonstrate the functional and anatomical diversity of tectal and reticular neurons, which are generally considered as homogeneous populations and used, accordingly, as lumped elements in models. We argue that the extraction of effector-specific signals from the global command of gaze displacement is based not on the interplay between discrete neural modules, but rather on a gradual process of signal specification at all levels of the executive network. An eventual accurate description of this network will require knowledge of the unique combinations of afferent inputs and efferent connections for as many subsets of its constituent neurons as is conceivably possible.

Arm movement metrics influence saccade metrics when looking and pointing towards a memorized target location

Saccades are known to influence subsequent arm movements. There is less information to suggest that the characteristics of saccades depend on the reaching movements they accompany. To explore this issue, we studied the systematic errors of saccades generated by two adult female Rhesus monkeys (Macaca Mulata), which were trained to perform center-out saccades and reaching arm movements to the memorized location of targets. The mean error of saccades executed in isolation differed significantly from that of saccades that were executed towards the same target location and accompanied a reaching movement. This difference was observed in both animals whether they used their right or left arm, whether the size of the movement was equal to 10 or 15xa0degrees and whether there was no delay or a 3xa0s delay between the extinction of a visual target and the cue to move. Moreover, the endpoints of saccades and those of the arm-reaching movements in the reaching task were significantly correlated. These data suggest that signals specifying the metrics of limb movements influence those specifying the metrics of preceding saccades at a programming stage.

Eye position modulates the electromyographic responses of neck muscles to electrical stimulation of the superior colliculus in the alert cat

Rapid gaze shifts are often accomplished with coordinated movements of the eyes and head, the relative amplitude of which depends on the starting position of the eyes. The size of gaze shifts is determined by the superior colliculus (SC) but additional processing in the lower brain stem is needed to determine the relative contributions of eye and head components. Models of eye–head coordination often assume that the strength of the command sent to the head controllers is modified by a signal indicative of the eye position. Evidence in favor of this hypothesis has been recently obtained in a study of phasic electromyographic (EMG) responses to stimulation of the SC in head-restrained monkeys (Corneil et al. in J Neurophysiol 88:2000–2018, 2002b). Bearing in mind that the patterns of eye–head coordination are not the same in all species and because the eye position sensitivity of phasic EMG responses has not been systematically investigated in cats, in the present study we used cats to address this issue. We stimulated electrically the intermediate and deep layers of the caudal SC in alert cats and recorded the EMG responses of neck muscles with horizontal and vertical pulling directions. Our data demonstrate that phasic, short latency EMG responses can be modulated by the eye position such that they increase as the eye occupies more and more eccentric positions in the pulling direction of the muscle tested. However, the influence of the eye position is rather modest, typically accounting for only 10–50% of the variance of EMG response amplitude. Responses evoked from several SC sites were not modulated by the eye position.

Response Properties of Motor Equivalence Neurons of the Primate Premotor Cortex

To study the response properties of cells that could participate in eye-hand coordination we trained two macaque monkeys to perform center-out saccades and pointing movements with their right or left forelimb toward visual targets presented on a video display. We analyzed the phasic movement related discharges of neurons of the periarcuate cortex that fire before and during saccades and movements of the hand whether accompanied by movements of the other effector or not. Because such cells could encode an abstract form of the desired displacement vector without regard to the effector that would execute the movement we refer to such cells as motor equivalence neurons (Meq). Most of them (75%) were found in or near the smooth pursuit region and the grasp related region in the caudal bank of the arcuate sulcus. The onset of their phasic discharges preceded saccades by about 70 ms and hand movements by about 150 ms and was often correlated to both the onset of saccades and the onset of hand movements. The on-direction of Meq cells was uniformly distributed without preference for ipsiversive or contraversive movements. In about half of the Meq cells the preferred direction for saccades was the preferred direction for hand movements as well. In the remaining cells the difference was considerable (>90 deg), and the on-direction for eye-hand movements resembled that for isolated saccades in some cells and for isolated hand movements in others. A three layer neural network model that used Meq cells as its input layer showed that the combination of effector invariant discharges with non-invariant discharges could help reduce the number of decoding errors when the network attempts to compute the correct movement metrics of the right effector.

Saccades evoked in response to electrical stimulation of the posterior bank of the arcuate sulcus

To test the hypothesis that the premotor cortex in and behind the caudal bank of the arcuate sulcus can generate saccades, we stimulated electrically the periarcuate region of alert rhesus monkeys. We were able to produce saccades from sites of the premotor cortex that were contiguous with the frontal eye fields and extended up to 2xa0mm behind the smooth pursuit area. However, premotor sites often elicited saccades with ipsiversive characteristic vectors, lower peak velocities, and flatter velocity profiles when compared to saccades evoked from the frontal eye field.

RESPONSE PROPERTIES OF SACCADE RELATED NEURONS OF THE POST-ARCUATE PREMOTOR CORTEX

We studied the phasic saccade-related discharges of single neurons (S neurons) of the premotor cortex of female rhesus monkeys, mostly in the caudal bank of the arcuate sulcus. As described in previous work from our laboratory (Neromyliotis E, Moschovakis AK. Front Behav Neurosci 11: 1-21, 2017), some of these cells emitted phasic discharges for coordinated movements of the eyes and hand as well as for movements of either effector executed in isolation (motor equivalence, Meq). Other cells (S) did not emit phasic discharges for hand movements unaccompanied by saccades. In contrast to frontal eye field (FEF) neurons, but similar to forelimb-related neurons (H neurons) and Meq cells, the discharges of S cells did not display contralateral bias; their on-directions were as likely to be ipsiversive as contraversive. Because the onset of their discharge preceded that of FEF neurons, S cells are unlikely to convey to their targets corollary discharges of the FEF. We also encountered a small number of neurons that could function as logic gates: cells that discharged for saccades if they were not accompanied by hand movements, cells that discharged for saccades or movements of the hand but not for coordinated movements of both effectors, and cells that discharged only for coordinated movements of the eyes and the hand but not when one of the effectors moved unaccompanied by the other. Our findings are discussed in terms of sequences of decision processes stitching effector-specific motor plans onto effector-invariant movement primitives. NEW & NOTEWORTHY The premotor cortex, traditionally associated with skeletomotor control, is shown to contain cells that emit strong discharges time-linked to saccades but not for hand movements unaccompanied by saccades (S cells). Unlike frontal eye field (FEF) neurons, the S cells of the premotor cortex did not display contralateral bias, and because their presaccadic discharges preceded those of FEF neurons, they are unlikely to serve as conveyors of FEF efferent discharges.