Tectal etiology for irrepressible saccades: a case study in a Rhesus monkey.

Brain circuits controlling eye movements are widely distributed and complex. The etiology of irrepressible square wave saccades is not fully understood and is likely different for different neuropathologies. In a previous study, spontaneously occurring irrepressible saccades were noted after a cerebrovascular accident that damaged the rostral superior colliculus (SC) and its commissure in a Rhesus monkey. Here, we tracked and quantified the development of similar symptoms in a Rhesus monkey caused by a lesion in the rostromedial SC and its commissure. We documented the changes in these saccadic intrusions while the monkey attempted fixation of a target on three consecutive days post-onset. On the first day, eye jerk amplitude was ~10 degrees and the direction was ~30 degrees above the left horizontal meridian. On the second day, the amplitude decreased to 6.5 degrees and the direction shifted towards vertical, ~20 degrees to the left of the vertical meridian. Size, but not direction, of the eye jerks continued to decrease until intrusions dissipated within one month. Histological examination after ~6 months from the first appearance of the intrusions revealed a lesion in the commissure of the SC. Results from this and the previous study confirm the involvement of the commissure of the SC as the common target for triggering this neuropathy. Our data suggest that commissural fibers play an important role in maintaining normal visual stability. Interrupting the commissure between the two superior colliculi causes saccadic intrusions in the form of irrepressible jerking of the eyes, probably by disrupting inhibitory signals transmitted through the commissure. Furthermore, disappearance of the symptoms suggests that inhibitory fields within the SC are plastic and can expand, possibly via inputs from inter-collicular and nigrotectal pathways.

A flexible user-interface for audiovisual presentation and interactive control in neurobehavioral experiments.

A major problem facing behavioral neuroscientists is a lack of unified, vendor-distributed data acquisition systems that allow stimulus presentation and behavioral monitoring while recording neural activity. Numerous systems perform one of these tasks well independently, but to our knowledge, a useful package with a straightforward user interface does not exist. Here we describe the development of a flexible, script-based user interface that enables customization for real-time stimulus presentation, behavioral monitoring and data acquisition. The experimental design can also incorporate neural microstimulation paradigms. We used this interface to deliver multimodal, auditory and visual (images or video) stimuli to a nonhuman primate and acquire single-unit data. Our design is cost-effective and works well with commercially available hardware and software. Our design incorporates a script, providing high-level control of data acquisition via a sequencer running on a digital signal processor to enable behaviorally triggered control of the presentation of visual and auditory stimuli. Our experiments were conducted in combination with eye-tracking hardware. The script, however, is designed to be broadly useful to neuroscientists who may want to deliver stimuli of different modalities using any animal model.

Saccade trajectories evoked by sequential and colliding stimulation of the monkey superior colliculus.

Using microstimulation we employed an explicit experimental control of activity in the superior colliculus at two sites within the motor map. We compared saccade metrics and dynamics evoked at each site independently with those caused by sequential presentation and collisions of the two stimulation trains. Essentially, we forced controlled spatio-temporal patterns of activity into the saccade control circuit with various timing relationships from known sites within the collicular motor map, thus revealing the spatio-temporal transformation from superior colliculus to eye movement dynamics under experimentally controlled conditions. We extend prior findings about decreasing time intervals between sequential presentations of stimulations to include mid-flight combinations and dynamic modifications of trajectory. We explore how asynchronous collisions between two movements systematically engage a normalization mechanism of movement metrics, and demonstrate how dynamic patterns of activity across the SC motor map can create mid-flight curvature of movement through the post-collicular dynamics of a displacement controller. The explicit control addresses feasibility for systems control models and provides benchmark data for experimental verification of model mechanisms.

Premotor inhibitory neurons carry signals related to saccade adaptation in the monkey.

Cerebellar output changes during motor learning. How these changes cause alterations of motoneuron activity and movement remains an unresolved question for voluntary movements. To answer this question, we examined premotor neurons for saccadic eye movement. Previous studies indicate that cells in the fastigial oculomotor region (FOR) within the cerebellar nuclei on one side exhibit a gradual increase in their saccade-related discharge as the amplitude of ipsiversive saccades adaptively decreases. This change in FOR activity could cause the adaptive change in saccade amplitude because neurons in the FOR project directly to the brain stem region containing premotor burst neurons (BNs). To test this possibility, we recorded the activity of saccade-related burst neurons in the area that houses premotor inhibitory burst neurons (IBNs) and examined their discharge during amplitude-reducing adaptation elicited by intrasaccadic target steps. We specifically analyzed their activity for off-direction (contraversive) saccades, in which the IBN activity would increase to reduce saccade size. Before adaptation, 29 of 42 BNs examined discharged, at least occasionally, for contraversive saccades. As the amplitude of contraversive saccades decreased adaptively, half of BNs with off-direction spike activity showed an increase in the number of spikes (14/29) or an earlier occurrence of spikes (7/14). BNs that were silent during off-direction saccades before adaptation remained silent after adaptation. These results indicate that the changes in the off-direction activity of BNs are closely related to adaptive changes in saccade size and are appropriate to cause these changes.

Effect of visual error size on saccade adaptation in monkey.

Saccades that consistently over- or undershoot their targets gradually become smaller or larger, respectively. The signal that elicits adaptation of saccade size is a difference between eye and target positions appearing repeatedly at the ends of saccades. Here we describe how visual error size affects the size of saccade adaptation. At the end of each saccade, we imposed a constant-sized error by moving the target to a specified point relative to eye position. We tested a variety of error sizes imposed after saccades to target movements of 6, 12, and 18 degrees. We found that the size of the gain change elicited in a particular experiment depended on both the size of the imposed postsaccade error and on the size of the preceding target movement. For example, imposed errors of 4-5 degrees reduce saccades tracking 6, 12, and 18 degrees target movements by an average of 18, 35, and 45%, respectively. The most effective errors were those that were 15-45% of the size of the initial target eccentricity. Negative errors, which reduce saccade size, were more effective in changing saccade gain than were positive errors, which increased saccade size. For example, for 12 degrees target movements, negative and positive errors of 2-6 degrees changed saccade gain an average of 35 and 8%, respectively. This description of the relationship between error size and adaptation size improves our ability to adapt saccades in the laboratory and characterizes the error sizes that will best drive neurons carrying the adaptation-related visual error signal.