V. Henn

Neuronal activity in the vestibular nuclei of the alert monkey during vestibular and optokinetic stimulation

SummaryRecordings from neurons of the vestibular nuclei were performed in alert monkeys. Type I and type II units were identified by rotating the monkey about a vertical axis. All neurons responded also when only the visual surround was rotated around the stationary monkey. The combination of visual and vestibular stimulation points towards non-algebraic summation characteristics for the two inputs, with each input dominating the response over a certain range.

Coding of information about rapid eye movements in the pontine reticular formation of alert monkeys.

Neurons in the rostral paramedian zone of the pontine reticular formation (PRF) have distinct frequency changes prior to and during quick eye movements, but generally little or no tonic activity associated with eye position. Evidence indicates that horizontal saccades and quick phases of nystagmus are generated in this region. Firing of units activated with eye movements (burst units) and of units which are inhibited (pause units) was analyzed. Eye movements were described by a vector having an amplitude (A) and an angle (a). These parameters were related to position changes in certain planes by the equation delta pos = A - cos alpha. In each of 80 cells in the PRF which were encountered, the activity could be related to some parameter of the above equation: change of position (delta pos), amplitude (A), or the cosine of the angle between the direction of movement and a reference direction (cos alpha). Units coding amplitude of eye movement or change in position in a particular plane conveyed the information by number of spikes. Units coding direction of movement did so by frequency. In many units, the information coding was precise so that the direction or amplitude of single eye movements could be predicted from the frequency changes of single units. In other units, this could be determined from averages of the frequency changes. Cells coding direction or change in position had frequency maxima only in planes corresponding to the pulling direction of the eye muscles. The results suggest that a vector description is not only a convenient mathematical tool, but is the way eye movements are coded in the PRF and possibly elsewhere in the central nervous system.

Vestibular nuclei activity during optokinetic after-nystagmus (OKAN) in the alert monkey

SummaryNeurons which receive an input from the horizontal semicircular canals were recorded from the vestibular nuclei in chronically prepared monkeys (Macaca mulatta) during optokinetic after-nystagmus (OKAN). In complete darkness the vestibular neurons showed activity changes which closely paralleled the strength of nystagmus. The activity of vestibular units returned to baseline levels of spontaneous discharge only when all after-nystagmus had ceased, or when it was inhibited by stationary visual stimuli. The possible role of vestibular neurons in the generation of OKAN and its significance in vestibulo-visual interaction is discussed.

Visual-vestibular Interaction in the Flocculus of the Alert Monkey*

SummaryNeuronal activity in the flocculus of alert Rhesus monkeys was recorded during vestibular stimulation (rotation of the monkey about a vertical axis in complete darkness), optokinetic stimulation (rotation of the visual surround around the stationary monkey), combined visual-vestibular stimulation (rotation of the monkey inside the stationary surround in the light), and conflicting visual-vestibular stimulation (rotation of the monkey together with the visual surround in the same direction). The input to the flocculus was recorded as non-Purkinje cell (non-P-cell) activity. Ninety per cent of the non-P-cells which were modulated during our stimulation paradigms carry information similar to that in the neurons of vestibular nuclei. This suggests that the main mossy fiber input to the flocculus originates in the vestibular nuclei. A second input of unknown origin conveys visual information about retinal slip. Thus, part of the flocculus — as further discussed elsewhere (Waespe and Henn 1981) — may be specialized to subserve visual-vestibular interaction to improve the nystagmus response.

The sleep-wake transition in the oculomotor system

SummaryEye and head position, EEG, and activity of oculomotor and vestibular neurons in the brain-stem were recorded during alertness and at the transition to light sleep. Characteristic changes of firing patterns were found in many neuronal populations at the sleep-wake transition and could be related to disruption of fixation and rapid and compensatory eye movement generation. Moto-neurons decreased their firing rate by 20 to 50%, and their eye velocity coding deteriorated. Burst neurons had a significant drop in maximum firing rates and often showed continuous activity unrelated to rapid eye movements, but responded to vestibular stimuli. Pause neurons went completely silent. Neurons in the vestibular nuclei often reduced their level of activity, but still responded qualitatively unchanged to semicircular canal stimulation. In the framework of current models of oculomotor organization, the sleep-wake transition can be interpreted as a non-equilibrium phase transition which is driven by specific inputs and nonspecific activating systems.

Static Roll and Pitch in the Monkey: Shift and Rotation of Listing's Plane

In three rhesus monkeys three-dimensional eye positions were measured with the dual search coil technique. Recordings of spontaneous eye movements were made in the light and in the dark, with the monkeys in different static roll or pitch positions. Eye positions were expressed as rotation vectors. In all static positions eye rotation vectors were confined to a plane, i.e. Listings plane was conserved. Tilt about the roll axis shifted the plane along this axis, i.e. a constant torsional component was added to all eye positions. Tilt about the pitch axis changed the pitch angle of Listings plane.

Spatio-temporal recoding of rapid eye movement signals in the monkey paramedian pontine reticular formation (PPRF)

SummaryThe integrity of the paramedian pontine reticular formation (PPRF) is necessary for the generation of rapid eye movements. The main saccade-related population is of the burst type with latencies between 0 and 40 ms preceding a saccade, and they can be divided into medium- and long-lead burst neurons. Burst neurons have predominantly spatially coded movement fields in the rostral PPRF, while in the caudal PPRF they increase their burst strength in temporal coding approximately in the pulling directions of extraocular eye muscles (i.e. almost horizontal or vertical). Both neuronal populations have ipsilateral on-directions and contain longlead burst neurons. In a quantitative analysis the firing patterns of long-lead burst neurons are compared to those of medium-lead burst neurons, which form the predominant output of the saccadic pulse generator to the motoneurons.The firing patterns of temporally coded long-lead bursters are similar to those of medium-lead bursters, except for earlier on-latencies, larger statistical fluctuations, and specializations for small or large saccades in oblique directions. The spatially coded burst neurons form a motor map of saccadic vectors. The diameter of their movement field is often about the size of the saccade vector, and they encode saccadic onset and duration. These results are consistent with a model for visual saccades in eye displacement coordinates, where the spatio-temporal recoding of horizontal eye movements is effected by long-lead burst neurons in the PPRF.

Projections from the superior colliculus motor map to omnipause neurons in monkey.

Descending projections from the superior colliculus (SC) motor map to the saccadic omnipause neurons (OPNs) were examined in monkeys by using anterograde transport of tritiated leucine. The SC was divided into three zones: the rostral pole of the motor map, a small horizontal saccade zone in central SC, and a large horizontal saccade zone in caudal SC. Tracer injections into the intermediate layers of the three zones led to different patterns of silver grain deposits in and around nucleus raphe interpositus (RIP), which contains the OPNs: 1) From the rostral pole of the motor map, coarse axon branches of the crossed predorsal bundle spread medially into the RIP, branched, and terminated predominantly unilaterally over cells on the same side. 2) From the small horizontal saccade zone, the axon branches were of a finer caliber and terminated diffusely in the RIP, mainly on the same side. 3) From the large horizontal saccade zone, no terminal labeling was found within the RIP. 4) From the rostral pole of the motor map and small horizontal saccade zone, fiber branches from the ipsilateral descending pathway terminated diffusely over RIP. 5) In addition, terminal labeling in reticulospinal areas of the pons and medulla increased in parallel with the size of the saccade according to the SC motor map. The results suggest that there are multiple projections directly onto OPNs from the rostral SC but not from the caudal SC associated with large gaze shifts. The efferents from the rostral pole of the motor map may subserve the suppression of saccades during visual fixation, and those from the small horizontal saccade zone could inhibit anatagonist premotor circuits. J. Comp. Neurol. 413:55–67, 1999.

Deficits in torsional and vertical rapid eye movements and shift of Listing's plane after uni- and bilateral lesions of the rostral interstitial nucleus of the medial longitudinal fasciculus

The rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) contains burst neurons whose activity precedes rapid eye movements with a vertical and/or torsional component. To ascertain their causal role in the generation of conjugate eye movements, we placed uni- and bilateral kainic acid lesions in that region. Unilateral inactivation of the riMLF leads to a loss of all rapid eye movements with an ipsitorsional component (ipsitorsional is defined as movement of the upper pole of the ipsilateral eye in a temporal direction). Vertical eye movements are impaired in an asymmetric way, with downward movements slowed and upward movements little affected. Listings plane is shifted in the contratorsional direction, i.e., we find a constant torsional offset for all eye positions. With bilateral lesions one observes a total loss of all vertical and torsional eye movements, while Listings plane retains its shape and position. These results show that burst neurons in the riMLF play a decisive role in generating rapid eye movements with a vertical and torsional component.

On the generation of vertical and torsional rapid eye movements in the monkey

SummaryThe role of the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) in generating the vertical and torsional components of rapid eye movements was examined. The on-directions of burst neurons in the riMLF of alert Rhesus monkeys were obtained during quick phase nystagmus in three dimensions. The distinguishing feature of these burst neurons was the torsional component of their on-directions; neurons on the right side exhibited a clockwise component, from the point of view of the subject, while those on the left had a counterclockwise component. Vertical components could have up or down directions. This organization was verified by means of unilateral reversible inactivation of the riMLF using Muscimol. An injection in the right riMLF impaired the generation of quick phases with clockwise components while one on the left impaired counterclockwise components.