Barry W. Peterson

Neck muscle activation patterns in humans during isometric head stabilization

SummaryA musculoskeletal system with more muscles than there are motions could be programmed in alternative ways to produce a single movement. In this case, the muscles would have the potential to be maximally responsive in multiple directions rather than responding preferentially in a single direction. To determine the response patterns of muscles in the head-neck motor system, the simultaneous activation of four of the 23 neck muscles acting on the head was recorded with both surface and intramuscular electrodes. Fifteen human subjects were tested during an isometric head stabilization task. When the EMG response patterns were plotted, each muscle demonstrated a preferred direction of activation. This preferred activation direction was consistent in all of the subjects for three of the muscles tested. The fourth muscle, splenius, was preferentially activated during neck flexion in half of the subjects and during neck extension in the other half. Increasing the force parameters of the task suggested a linear relationship between force and the EMG output in the preferred response directions. Responses in the nonpreferred directions were produced by a nonlinear change in EMG activation of the muscle. This finding could have implications for theories of how reciprocal activation and cocontraction patterns of response are elicited. Results from this study, that the CNS programs neck muscles to respond in specific orientations rather than generating an infinite variety of muscle patterns, are in agreement with our findings in the cat.

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.

Responses of ponto-medullary reticular neurons to cortical, tectal and cutaneous stimuli

SummaryResponses of neurons in the medial ponto-medullary reticular formation to cortical, tectal and cutaneous stimuli were studied in cerebellectomized cats under chloralose-urethan or pentobarbital anesthesia. Reticulospinal neurons were identified by their antidromic responses to stimulation of the cervical and lumbar spinal cord. The reticulospinal axons of neurons located in the caudal part of n.r. gigantocellularis tended to have slower conduction velocities than axons of neurons in more rostral regions.Stimuli applied to the deep layers of the superior colliculus and to the pericruciate cortex or cerebral peduncles evoked monosynaptic EPSPs in many reticular neurons including reticulospinal neurons. Cutaneous stimuli evoked polysynaptic EPSPs or IPSPs. A prolonged period of depression that appeared to be caused by disfacilitation often followed the initial PSPs.Investigation of the origin of tecto-reticular excitation by means of movable stimulating electrodes revealed that excitation of contralateral reticular neurons was evoked by activation of elements within the tectum whereas excitation produced in ipsilateral reticular neurons may have involved activation of laterally situated, sub-tectal elements. The properties of reticular responses to tectal stimuli suggest that reticular neurons may act as relays between the tectum and neck motoneurons and possibly other spinal motoneurons as well.Investigation of the convergence of different inputs upon individual reticular neurons revealed a significant positive correlation between responses to stimulation of different tectal points and between responses to stimulation of ipsi- and contralateral pericruciate cortex but no correlation between responses to stimuli of different types.

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.

Coding of smooth eye movements in three-dimensional space by frontal cortex

Through the development of a high-acuity fovea, primates with frontal eyes have acquired the ability to use binocular eye movements to track small objects moving in space. The smooth-pursuit system moves both eyes in the same direction to track movement in the frontal plane (frontal pursuit), whereas the vergence system moves left and right eyes in opposite directions to track targets moving towards or away from the observer (vergence tracking). In the cerebral cortex and brainstem, signals related to vergence eye movements—and the retinal disparity and blur signals that elicit them—are coded independently of signals related to frontal pursuit. Here we show that these types of signal are represented in a completely different way in the smooth-pursuit region of the frontal eye fields. Neurons of the frontal eye field modulate strongly during both frontal pursuit and vergence tracking, which results in three-dimensional cartesian representations of eye movements. We propose that the brain creates this distinctly different intermediate representation to allow these neurons to function as part of a system that enables primates to track and manipulate objects moving in three-dimensional space.

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.

A dynamical model for reflex activated head movements in the horizontal plane.

Abstract. We present a controls systems model of horizontal-plane head movements during perturbations of the trunk, which for the first time interfaces a model of the human head with neural feedback controllers representing the vestibulocollic (VCR) and the cervicocollic (CCR) reflexes. This model is homeomorphic such that model structure and parameters are drawn directly from anthropomorphic, biomechanical and physiological studies. Using control theory we analyzed the system model in the time and frequency domains, simulating neck movement responses to input perturbations of the trunk. Without reflex control, the head and neck system produced a second-order underdamped response with a 5.2 dB resonant peak at 2.1 Hz. Adding the CCR component to the system dampened the response by approximately 7%. Adding the VCR component dampened head oscillations by 75%. The VCR also improved low-frequency compensation by increasing the gain and phase lag, creating a phase minimum at 0.1 Hz and a phase peak at 1.1 Hz. Combining all three components (mechanics, VCR and CCR) linearly in the head and neck system reduced the amplitude of the resonant peak to 1.1 dB and increased the resonant frequency to 2.9 Hz. The closed loop results closely fit human data, and explain quantitatively the characteristic phase peak often observed.

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.