Albert F. Fuchs

The neuronal substrate of integration in the oculomotor system

Abbreviations

Influence of stimulus parameters on visual sensitivity during saccadic eye movement

Abstract Visual threshold for stroboscope test flashes was measured during saccadic eye movements over various backgrounds and compared with measures obtained during eye fixation when the same backgrounds were “saccadically” displaced. Amount and time course of threshold change in the two situations compared well, suggesting no necessity for corollary discharge or other oculomotor interference with primary visual processes during eye movement. No significant threshold rise took place during saccades in the dark. Diffuse test flashes and small well focused flashes were affected differently by specific background conditions. Diffuse flashes were perceived with more difficulty during a saccade over a contour-free background than well focused, punctate stimuli. On the other hand, contours in the background raised saccadic thresholds for small stimuli much more than for diffuse test flashes. All threshold changes occurring during saccades were accentuated by increasing the background luminance.

Complex Spike Activity of Purkinje Cells in the Oculomotor Vermis during Behavioral Adaptation of Monkey Saccades

Throughout life, the oculomotor system can correct itself when saccadic eye movements become inaccurate. This adaptation mechanism can be engaged in the laboratory by displacing the target when the saccade toward it is in flight. Forward and backward target displacements cause gradual increases and decreases in saccade amplitude, respectively. Equipped with this paradigm, we asked whether Purkinje cells (P-cells) in the vermis of the oculomotor cerebellum, lobules VIc and VII, changed their complex spike (CS) discharge during the behavioral adaptation of horizontal saccades. We tested the hypothesis that CS activity would change only when a targeting saccade caused an error in eye position relative to the target, i.e., during the error interval between the primary and corrective saccades. We examined only those P-cells whose simple spike activity exhibited either a burst or pause with saccades in several directions. Approximately 80% of such P-cells exhibited an increase in CS activity during the error interval when the adaptation paradigm imposed horizontal eye-position errors in one direction and a decrease in activity for errors in the other. As adaptation progressed and errors were reduced, there was no consistent change in the CS activity. These data suggest that the CS activity of P-cells in the oculomotor vermis signals the direction but not the magnitude of eye-position error during saccade adaptation. Our results are consistent with cerebellar learning models that have been proposed to explain adaptation of the vestibulo-ocular reflex so similar mechanisms may also underlie plasticity of this precision voluntary oculomotor behavior.

Bilateral lesions of the medial longitudinal fasciculus in monkeys: effects on the horizontal and vertical components of voluntary and vestibular induced eye movements.

SummaryBilateral transections across the brainstem interrupted the medial longitudinal fasciculus (MLF) in three monkeys trained to make eye movements while subjected to horizontal or vertical angular accelerations. Eye movements measured before and after the lesion revealed deficits in both voluntary and vestibular compensatory eye movements; the deficits differed in the horizontal and vertical directions. Vertical saccades in both directions were normal but eccentric positions of fixation could not be maintained; a drift toward the midline followed by a corrective saccade produced vertical fixation nystagmus. Furthermore, the vertical vestibuloocular reflex (VOR) was abolished and vertical smooth pursuit was impaired. Along the horizontal meridian, adduction across the midline could not be achieved during either saccades, smooth pursuit, or the VOR. Temporal saccades were normal whereas nasal saccades were considerably slowed. If the eye was not required to cross the midline, the phase shift during the VOR was within 15 deg of normal in each eye. The gain of the VOR was reduced to about 0.4 immediately after the lesion, but recovered within one month. These findings suggest that the MLF transmits quite different kinds of information to horizontal and vertical oculomotoneurons and that deficits in vertical eye movements may be a sensitive indicator of anterior internuclear ophthalmoplegia.

Effect of mean reaction time on saccadic responses to two-step stimuli with horizontal and vertical components.

Abstract Saccadic responses to target movements containing two horizontal, two vertical and paired horizontal-vertical steps were measured in three human subjects. In all three target conditions, subjects made predominantly one saccade for short interstep intervals (ISI) and two saccades for long ISIs. However, the percentage of two-saccade responses (% 2 saccades) at each ISI varied substantially among target conditions and subjects due to inter-experiment variability in mean single step reaction times ( RT ). Correlation of % 2 saccades with the normalized interval RT minus ISI reduced interexperiment variability and suggested a sigmoid curve that applied to all our subjects and most other data taken from the literature.

Cerebellar influences on saccade plasticity.

Abstract: Inaccurate saccades adapt to become more accurate. In this experiment the role of cerebellar output to the oculomotor system in adapting saccade size was investigated. We measured saccade adaptation after temporary inactivation of saccade‐related neurons in the caudal part of the fastigial nucleus which projects to the oculomotor brain stem. We located caudal fastigial nucleus neurons with single unit recording and injected 0.1% muscimol among them. Two monkeys received bilateral injections and two monkeys unilateral injections. Unilateral injections made ipsiversive saccades hypermetric (gains >1.5) and contraversive saccades hypometric (gains ∼0.6). Bilateral injections made both leftward and rightward saccades hypermetric (gains >1.5). During unilateral inactivation neither ipsiversive nor contraversive saccade size adapted after ∼1,000 saccades. During bilateral inactivation, adaptation was either small or very slow. Most intact monkeys completely adapt after ∼1,000 saccades to similar dysmetrias produced by intrasaccadic target displacement. After the monkeys receiving bilateral injections made >1,000 saccades in each horizontal direction, we placed them in the dark so that the muscimol dissipated without the monkeys receiving visual feedback about its saccade gain. After the dark period, 20‐degree saccades were adapted to be 12% smaller, and 4‐degree saccades to be 7% smaller. We expect this difference in adaptation because during caudal fastigial nucleus inactivation, monkeys made many large overshooting saccades and few small overshooting saccades. We conclude from these results that: (1) caudal fastigial nucleus activity is important in adapting dysmetric saccades; and (2) bilateral caudal fastigial nucleus inactivation impairs the relay of adapted signals to the oculomotor system, but it does not stop all adaptation from occurring.

Complex spike activity in the oculomotor vermis of the cerebellum: a vectorial error signal for saccade motor learning?

Brain stem signals that generate saccadic eye movements originate in the superior colliculus. They reach the pontine burst generator for horizontal saccades via short-latency pathways and a longer pathway through the oculomotor vermis (OMV) of the cerebellum. Lesion studies implicate the OMV in the adaptation of saccade amplitude that occurs when saccades become inaccurate because of extraocular muscle weakness or behavioral manipulations. We studied the nature of the possible error signal that might drive adaptation by examining the complex spike (CS) activity of vermis Purkinje (P-) cells in monkeys. We produced a saccade error by displacing the target as a saccade was made toward it; a corrective saccade approximately 200 ms later eliminated the resulting error. In most P-cells, the probability of CS firing changed, but only in the error interval between the primary and corrective saccade. For most P-cells, CSs occurred in a tight cluster approximately 100 ms after error onset. The probability of CS occurrence depended on both error direction and size. Across our sample, all error directions were represented; most had a horizontal component. In more than one half of our P-cells, the probability of CS occurrence was greatest for error sizes<5 degrees and less for larger errors. In the remaining cells, there was a uniform increased probability of CS occurrence for all errors<or=7-9 degrees. CS responses disappeared when the target was extinguished during a saccade. We discuss the properties of this putative CS error signal in the context of the characteristics of saccade adaptation produced by the target displacement paradigm.

Discharge properties of neurons in the monkey thalamus tested with angular acceleration, eye movement and visual stimuli.

SummaryMonkeys were trained to make visually evoked eye movements while undergoing simultaneous head rotation. Single units were recorded in the pregeniculate nucleus (PGN). PGN neurons discharged during each saccade, but there was no change in activity with horizontal head acceleration or with various combinations of head and smooth pursuit eye movements as previously described in the cat. Therefore, the anatomical homology between LGNv and PGN does not appear to have a neurophysiological basis. Neurons in the oral part of VPL or occasionally in VPI discharged as a function of head velocity but not with saccades, smooth pursuit or fixation eye movements, nor after brief light flashes or during smooth pursuit across structured backgrounds. This suggests that VPLo and VPI are only vestibular relay nuclei and not concerned with vestibular/visual or vestibular/oculomotor interactions.It is a pleasure to acknowledge the histological talents of Donna Simmons, the veterinary care provided by Stan Crossman and Margaret Price, the surgical assistance of Doug Hasund, the secretarial help of Jean Scalf, and the editorial comments of Kate Schmitt.

Changes in Simple Spike Activity of Some Purkinje Cells in the Oculomotor Vermis during Saccade Adaptation Are Appropriate to Participate in Motor Learning

Adaptation of saccadic eye movements provides an excellent motor learning model to study theories of neuronal plasticity. When primates make saccades to a jumping target, a backward step of the target during the saccade can make it appear to overshoot. If this deception continues for many trials, saccades gradually decrease in amplitude to go directly to the back-stepped target location. We used this adaptation paradigm to evaluate the Marr–Albus hypothesis that such motor learning occurs at the Purkinje (P)-cell of the cerebellum. We recorded the activity of identified P-cells in the oculomotor vermis, lobules VIc and VII. After documenting the on and off error directions of the complex spike activity of a P-cell, we determined whether its saccade-related simple spike (SS) activity changed during saccade adaptation in those two directions. Before adaptation, 57 of 61 P-cells exhibited a clear burst, pause, or a combination of both for saccades in one or both directions. Sixty-two percent of all cells, including two of the four initially unresponsive ones, behaved differently for saccades whose size changed because of adaptation than for saccades of similar sizes gathered before adaptation. In at least 42% of these, the changes were appropriate to decrease saccade amplitude based on our current knowledge of cerebellum and brainstem saccade circuitry. Changes in activity during adaptation were not compensating for the potential fatigue associated with performing many saccades. Therefore, many P-cells in the oculomotor vermis exhibit changes in SS activity specific to adapted saccades and therefore appropriate to induce adaptation.

Oblique saccadic eye movements of the cat

SummaryA quantitative study of saccadic eye movements in the cat was undertaken to attempt to account for the high degree of variability in the trajectory of feline saccades compared with the more stereotyped monkey saccades. Cats were trained to make oblique saccades so that a large variety of saccadic component amplitudes, maximum velocities, and durations could be obtained.The horizontal and vertical components of oblique saccades were either stretched or compressed, relative to equal amplitude movements without orthogonal components, so that the two components were nearly equal in duration. On average, the components began approximately synchronously but were more asynchronous in their termination times. Consistent with the stretching or compression of a saccadic component, there was the complementary decrease or increase respectively of its maximum velocity. The product of maximum velocity and duration was constant for saccades of a given size. Furthermore, the constant relating maximum velocity and duration was a linear function of saccade size. Therefore, any saccade size was uniquely determined by knowing both duration and maximum velocity while knowing either alone resulted in considerable ambiguity in specifying saccade size.In addition to uniquely specifying feline saccades with different degrees of obliquity, this two parameter description allowed us to fit not only the monkey data but data obtained from rabbit and human as well. Therefore, specification of both duration and maximum velocity might be a basic organizing principle of the neural mechanisms generating saccades in many species.