James F. Baker

Spatial and temporal response properties of secondary neurons that receive convergent input in vestibular nuclei of alert cats

Responses to rotation in many vertical and horizontal planes were studied in electrically identified secondary vestibular neurons of alert cats. This report concerns secondary neurons that gave responses which could not be explained as due to a summation of semicircular canal inputs. These cells responded to sinusoidal rotation of the cat in any vertical plane, and response phase depended on the plane of rotation. The responses were modeled as the result of summation of two inputs that differed in their spatial orientations and dynamics. Response dynamics and a comparison of responses to vertical and horizontal rotations showed that some cells were sensitive to rotation with respect to gravity. Their responses both to gravity and horizontal rotations argue that these secondary neurons received convergent otolith and canal inputs. Some cells also had oculomotor related discharges and/or responded weakly to neck rotation.

Spatial properties of second-order vestibulo-ocular relay neurons in the alert cat.

SummarySecond-order vestibular nucleus neurons which were antidromically activated from the region of the oculomotor nucleus (second-order vestibuloocular relay neurons) were studied in alert cats during whole-body rotations in many horizontal and vertical planes. Sinusoidal rotation elicited sinusoidal modulation of firing rates except during rotation in a clearly defined null plane. Response gain (spikes/s/deg/s) varied as a cosine function of the orientation of the cat with respect to a horizontal rotation axis, and phases were near that of head velocity, suggesting linear summation of canal inputs. A maximum activation direction (MAD) was calculated for each cell to represent the axis of rotation in three-dimensional space for which the cell responded maximally. Second-order vestibuloocular neurons divided into 3 non-overlapping populations of MADs, indicating primary canal input from either anterior, posterior, or horizontal semicircular canal (AC, PC, HC cells). 80/84 neurons received primary canal input from ipsilateral vertical canals. Of these, at least 6 received input from more than one vertical canal, suggested by MAD azimuths which were sufficiently misaligned with their primary canal. In addition, 21/80 received convergent input from a horizontal canal, with about equal number of type I and type II yaw responses. 4/84 neurons were HC cells; all of them received convergent input from at least one vertical canal. Activity of many vertical second-order vestibuloocular neurons was also related to vertical and/or horizontal eye position. All AC and PC cells that had vertical eye position sensitivity had upward and downward on-directions, respectively. A number of PC cells had MADs centered around the MAD of the superior oblique muscle, and 2/3 AC cells recorded in the superior vestibular nucleus had MADs near that of the inferior oblique. Thus, signals with spatial properties appropriate to activate oblique eye muscles are present at the second-order vestibular neuron level. In contrast, none of the second-order vestibuloocular neurons had MADs near those of the superior or inferior rectus muscles. Signals appropriate to activate these eye muscles might be produced by combining signals from ipsilateral and contralateral AC neurons (for superior rectus) or PC neurons (for inferior rectus). Alternatively, less direct pathways such as those involving third or higher order vestibular or interstitial nucleus of Cajal neurons might play a crucial role in the spatial transformations between semicircular canals and vertical rectus eye muscles.

The latency of the cat vestibulo-ocular reflex before and after short- and long-term adaptation

Latencies of normal and adapted feline vestibulo-ocular reflex (VOR) were studied in five cats by applying ± 20°/s horizontal head velocity steps (4000°/s2 acceleration) and measuring the elicited horizontal or vertical reflex eye responses. Normal VOR latency was 13.0 ms ± 1.9 SD. Short-term adaptation was then accomplished by using 2 h of paired horizontal sinusoidal vestibular stimulation and phase-synchronized vertical optokinetic stimulation (cross-axis adaptation). For long-term adaptation, cats wore ×0.25 or ×2.2 magnifying lenses for 4 days. The cats were passively rotated for 2 h/day and allowed to walk freely in the laboratory or their cages for the remainder of the time. The latency of the early (primary) adaptive response was 15.2ms±5.2 SD for crossaxis adaptation and 12.5 ms±3.9 SD for lens adaptation. This short-latency response appeared within 30 min after beginning the adaptation procedure and diminished in magnitude overnight. A late (secondary) adaptive response with latency of 76.8 ms±7.0 SD for cross-axis adaptation and 68.1 ms±8.8 SD for lens adaptation appeared after approximately 2 h of adaptation. It had a more gradual increase in magnitude than the primary response and did not diminish in magnitude overnight. These data suggest that brainstem VOR pathways are a site of learning for adaptive VOR modification, since the primary latency is short and has a similar latency to that of the normal VOR.

Optimal response planes and canal convergence in secondary neurons in vestibular nuclei of alert cats

Responses to natural stimulation were studied in electrically identified secondary vestibular neurons of awake cats. A class of neurons was identified whose response dynamics and responses to rotations in several vertical and horizontal planes indicated that they received semicircular canal input. Each canal neuron had clearly defined planes of maximal and null sensitivity to rotation. The orientation of these planes indicated that 44% of the neurons received input from one pair of canals, 40% from two, and 16% from all 3 canal pairs. Many cells also had oculomotor-related discharges and/or responded weakly to neck rotation.

Simultaneous opposing adaptive changes in cat vestibulo-ocular reflex direction for two body orientations

SummaryThe specificity of adaptation of vestibuloocular reflex direction was examined by exposing cats to combined pitch vestibular rotation and horizontal optokinetic motion at 0.25 Hz, while alternating body position between lying on the left side and lying on the right. The direction of optokinetic motion relative to head motion was reversed when the cats body posture was changed so that, for example, if head upward rotation was coupled to leftward visual world motion when the cat was lying on its left side, then head upward rotation was coupled to rightward visual world motion when the cat was on its right side. Body position and optokinetic motion direction were changed every 10 min for a total of 2 h of adaptation on each side. Horizontal and vertical electrooculographic recordings were made during pitch rotations in darkness before and after adaptation. Saccades were removed from the records and vestibulo-ocular reflex gain was measured in the direction of optokinetic motion. In every case, the adaptation procedure produced a directional change in the vestibulo-ocular reflex specific to the posture during measurement and appropriate to reduce the retinal image motion caused by the combined vestibular and optokinetic stimuli. That is, adaptive horizontal eye movements measured on the two sides were in opposite directions for the same direction of head motion. This specificity suggests that adaptation of vestibulo-ocular reflex direction involves specific neural pathways that are controlled by body orientation signals which most likely arise from the otolith organs.

Oculomotor reflexes after semicircular canal plugging in cats

The horizontal ocular reflexes of cats were studied before and after plugging all 6 semicircular canals (2 cats) or the horizontal canals only (2 cats). After plugging, the vestibulo-ocular reflex (VOR) was virtually absent in the cats with all canals plugged; a small phase-advanced VOR was detectable only at high velocities of rotation. There was no VOR recovery over several months. A compensatory cervico-ocular reflex (COR) appeared within a few days of plugging in all cats, and increased in gain slowly over time. The cats with horizontal canals plugged had little VOR during yaw rotation with the head pitched near 30 degrees down from the stereotaxic plane. When the head was pitched nose up from this null plane, a horizontal VOR appeared and increased as the sine of pitch angle, indicating that the cats relied on normal or increased coupling of vertical canals to horizontal eye movers for generation of compensatory eye movements. Periods of compensatory and anticompensatory eye movements were recorded during downward pitched yaw.

Patterns of neck muscle activation in cats during reflex and voluntary head movements

SummaryWhen the head rotates, vestibulocollic reflexes counteract the rotation by causing contraction of the neck muscles that pull against the imposed motion. With voluntary head rotations, these same muscles contract and assist the movement of the head. The purpose of this study was to determine if an infinite variety of muscle activation patterns are available to generate a particular head movement, or if the CNS selects a consistent and unique muscle pattern for the same head movement whether performed in a voluntary or reflex mode. The relationship of neck muscle activity to reflex and voluntary head movements was examined by recording intramuscular EMG activity from six neck muscles in three alert cats during sinusoidal head rotations about 24 vertical and horizontal axes. The cats were trained to voluntarily follow a water spout with their heads. Vestibulocollic reflex (VCR) responses were recorded in the same cats by rotating them in an equivalent set of planes with the head stabilized to the trunk so that only the vestibular labyrinths were stimulated. Gain and phase of the EMG responses were calculated, and data analyzed to determine the directions of rotation for which specific muscles produced their greatest EMG output. Each muscle exhibited preferential activation for a unique direction of rotation, and weak responses during rotations orthogonal to that preferred direction. The direction of maximal activation could differ for reflex and voluntary responses. Also, the best excitation of the muscle was not always in the direction that would produce a maximum mechanical advantage for the muscle based on its line of pull. The results of this study suggest that a unique pattern of activity is selected for VCR and tracking responses in any one animal. Patterns for the two behaviors differ, indicating that the CNS can generate movements in the same direction using different muscle patterns.

Dependence of cat vestibulo-ocular reflex direction adaptation on animal orientation during adaptation and rotation in darkness

Four series of experiments investigated how adaptive changes in direction of the cats vestibulo-ocular reflex (VOR) vary with position of the animal during adaptive training and postadaptive testing. In all experiments VOR was measured electrooculographically during rotations about earth-horizontal and vertical axes in the dark before and after 2 h of adaptation in which 0.25 Hz sinusoidal whole body rotation about a horizontal/vertical axis was paired with synchronous 0.25 Hz rotation of a visual pattern about a vertical/horizontal axis, respectively. In upright sagittal (US) experiments, coupling of pitch rotation with visual pattern rotation about an earth vertical axis yielded an adaptive horizontal VOR response to pitch rotation whose gain had a local maximum at 0.25-0.5 Hz plus a sustained rise for frequencies below 0.1 Hz. When post-tests were done with the animal rolled 90 degrees onto its side and rotated about the earth vertical axis (pitch relative to the cat), the low frequency rise was eliminated and the 0.25 Hz peak was reduced. In on side sagittal (SS) experiments, where training was done in the latter (on side) position, training produced only the 0.25 Hz peak without the low frequency rise, indicating that the rise is due to coupling of otolith input to horizontal VOR. Again the 0.25 Hz peak was reduced when testing was done with the cat oriented 90 degrees from the training position (in the US position). This indicates that the cross-coupled canal-ocular reflex response is modulated or gated by the position of the animal with respect to gravity.(ABSTRACT TRUNCATED AT 250 WORDS)

TORQUE VECTORS OF NECK MUSCLES IN THE CAT

SummaryAnatomical texts describe the neck musculature without measurements of muscle locations or quantitative estimates of pulling actions (torques). This study is based on measurements in stereotaxic coordinates of cat neck muscle origins and insertions, and neck intervertebral rotation axes. Torque vectors in three dimensions were calculated for 14 pairs of dorsal and ventral muscles that insert on the skull or first cervical vertebra. Predicted torque vectors were in general agreement with qualitative statements in the literature. Biventer cervicis and the rectus capitis major, medius, and minor muscles act mainly to raise the head, and longus capitis acts almost exclusively to lower the head. Longissimus capitis, sternomastoid, and cleidomastoid act mainly to roll the head. Complexus acts about equally to raise the head and roll it. Splenius and occipitoscapularis have torque in all three coordinate directions. Torques were altered by changing the pitch of the head with respect to the neck. The calculated neck muscle torques did not correspond to previously reported directions of neck muscle excitation during the vestibulocollic reflex. The neck musculature appears to be a complex, multidimensional system that presents interesting problems in motor control.

Dynamic otolith stimulation improves the low frequency horizontal vestibulo-ocular reflex

SummaryThe horizontal vestibulo-ocular reflex was measured electrooculographically in four cats during sinusoidal rotations in the dark at frequencies from 0.01 Hz to 1.0 Hz in five body orientations. Vertical axis rotations in the prone and supine positions were used to stimulate horizontal canals only. Horizontal axis rotations, with the cat on the left or right side or nose down (pitched 90° from prone) were used to stimulate horizontal canal plus otolith organs. At frequencies below 0.05 Hz the horizontal vestibulo-ocular reflex produced by horizontal canal plus otolith stimulation showed a more accurately compensatory response than the horizontal vestibuloocular reflex produced by horizontal canal stimulation alone. Canal plus otolith horizontal vestibulo-ocular reflex gain and phase remained relatively constant across all frequencies, while the horizontal vestibulo-ocular reflex gain and phase from orientations involving canal stimulation alone changed dramatically as rotation frequency decreased. In addition, the reflex in the supine position showed gain decreases and phase advances at higher frequencies than in the prone position.