Neural Control of Superficial and Deep Neck Muscles in Humans

Human neck muscles have a complex multi-layered architecture. The role and neural control of these neck muscles were examined in nine seated subjects performing three series of isometric neck muscle contractions: 50-N contractions in eight fixed horizontal directions, 25-N contractions, and 50-N contractions, both with a continuously changing horizontal force direction. Activity in the left sternocleidomastoid, trapezius, levator scapulae, splenius capitis, semispinalis capitis, semispinalis cervicis, and multifidus muscles was measured with wire electrodes inserted at the C4/C5 level under ultrasound guidance. We hypothesized that deep and superficial neck muscles would function as postural and focal muscles, respectively, and would thus be controlled by different neural signals. To test these hypotheses, electromyographic (EMG) tuning curves and correlations in the temporal and frequency domains were computed. Three main results emerged from these analyses: EMG tuning curves from all muscles exhibited well-defined preferred directions of activation for the 50-N isometric forces, larger contractions (25 vs. 50 N) yielded more focused EMG tuning curves, and agonist neck muscles from all layers received a common neural drive in the range of 10–15 Hz. The current results demonstrate that all neck muscles can exhibit phasic activity during isometric neck muscle contractions. Similar oscillations in the EMG of neck muscles from different layers further suggest that neck motoneurons were activated by common neurons. The reticular formation appears a likely generator of the common drive to the neck motoneurons due to its widespread projections to different groups of neck motoneurons.

Dissociation of Eye and Head Components of Gaze Shifts by Stimulation of the Omnipause Neuron Region

Natural movements often include actions integrated across multiple effectors. Coordinated eye-head movements are driven by a command to shift the line of sight by a desired displacement vector. Yet because extraocular and neck motoneurons are separate entities, the gaze shift command must be separated into independent signals for eye and head movement control. We report that this separation occurs, at least partially, at or before the level of pontine omnipause neurons (OPNs). Stimulation of the OPNs prior to and during gaze shifts temporally decoupled the eye and head components by inhibiting gaze and eye saccades. In contrast, head movements were consistently initiated before gaze onset, and ongoing head movements continued along their trajectories, albeit with some characteristic modulations. After stimulation offset, a gaze shift composed of an eye saccade, and a reaccelerated head movement was produced to preserve gaze accuracy. We conclude that signals subject to OPN inhibition produce the eye-movement component of a coordinated eye-head gaze shift and are not the only signals involved in the generation of the head component of the gaze shift.

Transmission through the Dorsal Spinocerebellar and Spinoreticular Tracts

Background Most of what is known regarding the actions of injectable barbiturate anesthetics on the activity of lumbar sensory neurons arises from experiments performed in acute animal preparations that are exposed to invasive surgery and neural depression caused by coadministered inhalational anesthetics. Other parameters such as cortical synchronization and motor ouflow are typically not monitored, and, therefore, anesthetic actions on multiple cellular systems have not been quantitatively compared. Methods The activities of antidromically identified dorsal spinocerebellar and spinoreticular tract neurons, neck motoneurons, and cortical neurons were monitored extracellularly before, during, and following recovery from the anesthetic state induced by thiopental in intact, chronically instrumented animal preparations. Results Intravenous administration of 15 mg/kg, but not 5 mg/kg, of thiopental to awake cats induced general anesthesia that was characterized by 5-10 min of cortical synchronization, reflected as large-amplitude slow-wave events and neck muscle atonia. However, even though the animal behaviorally began to reemerge from the anesthetic state after this 5-10-min period, neck muscle (neck motoneuron) activity recovered more slowly and remained significantly suppressed for up to 23 min after thiopental administration. The spontaneous activity of both dorsal spinocerebellar and spinoreticular tract neurons was maximally suppressed 5 min after administration but remained significantly attenuated for up to 17 min after injection. Peripheral nerve and glutamate-evoked responses of dorsal spinocerebellar and spinoreticular tract neurons were particularly sensitive to thiopental administration and remained suppressed for up to 20 min after injection. Conclusions These results demonstrate that thiopental administration is associated with a prolonged blockade of motoneuron output and sensory transmission through the dorsal spinocerebellar and spinoreticular tracts that exceeds the duration of general anesthesia. Further, the blockade of glutamate-evoked neuronal responses indicates that these effects are due, in part, to a local action of the drug in the spinal cord. The authors suggest that this combination of lumbar sensory and motoneuron inhibition underlies the prolonged impairment of reflex coordination observed when thiopental is used clinically.

Input Patterns and Pathways From the Six Semicircular Canals to Motoneurons of Neck Muscles. II. The Longissimus and Semispinalis Muscle Groups

Shinoda, Y., Y. Sugiuchi, T. Futami, N. Ando, and J. Yagi. Input patterns and pathways from the six semicircular canals to motoneurons of neck muscles. II. The longissimus and semispinalis muscle groups. J. Neurophysiol. 77: 1234–1253, 1997. To reveal patterns of input from the six semicircular canals to motoneurons of various neck muscles and their relationship to the mechanical actions of individual neck muscles, patterns of input to neck motoneurons of the longissimus and the semispinalis muscle groups were investigated in the upper cervical spinal cord of anesthetized cats. Intracellular potentials were recorded from motoneurons of the longissimus muscle group (obliquus capitis superior muscle, OCS; splenius muscle, SPL; longissimus muscle, LONG) and the semispinalis muscle group (biventer cervicis muscle, BIV; complexus muscle, COMP), and effects of separate electrical stimulation of the six ampullary nerves on them were analyzed in each preparation. Neck motoneurons usually received convergent inputs from all of the six ampullary nerves, and motoneurons that supplied a particular muscle had a homogeneous pattern of input from the six ampullary nerves. Two different patterns of input were identified for motoneurons of these two muscle groups; one pattern for motoneurons of the longissimus muscle group and the other pattern for motoneurons of the semispinalis muscle group. Motoneurons of the OCS, the SPL, and the LONG muscles received excitation from the three contralateral ampullary nerves and inhibition from the three ipsilateral ampullary nerves. BIV and COMP motoneurons received excitation from the bilateral anterior canal nerves (ACNs) and the contralateral lateral canal nerve (LCN) and inhibition from the bilateral posterior canal nerves (PCNs) and the ipsilateral LCN. Latencies of postsynaptic potentials (PSPs) evoked by stimulation of each of the six ampullary nerves indicated that the earliest component of excitatory PSPs (EPSPs) and inhibitory PSPs (IPSPs) was disynaptic in these motoneurons. However, trisynaptic IPSPs were evoked by stimulation of the contralateral PCN in a considerable number of BIV and COMP motoneurons. In OCS, SPL, and LONG motoneurons, all of the excitation from the contralateral and all of the inhibition from the ipsilateral ampullary nerves were mediated through the ipsilateral medial longitudinal fascicle (MLF). In BIV and COMP motoneurons, disynaptic excitation from the contralateral ACN and LCN and disynaptic inhibition from the ipsilateral LCN and bilateral PCNs were mediated through the ipsilateral MLF, whereas disynaptic excitation from the ipsilateral ACN was mediated through the ipsilateral lateral vestibulospinal tract. The patterns of semicircular canal input to neck motoneurons of these two muscle groups are related closely to the mechanical actions of individual neck muscles and the optimal stimulus to the semicircular canals such that the connections will tend to stabilize head position in response to head perturbations.

Contribution of Voltage-Dependent Potassium Channels to the Somatic Shunt in Neck Motoneurons of the Cat

Campbell, D. M. and P. K. Rose. Contribution of voltage-dependent potassium channels to the somatic shunt in neck motoneurons of the cat. J. Neurophysiol. 77: 1470–1486, 1997. The specific membrane resistivity of motoneurons at or near the soma ( R ms) is much lower than the specific membrane resistivity of the dendritic tree ( R md). The goal of the present experiments was to investigate the contribution of tonically active voltage-dependent potassium channels at or near the soma to the low R ms. These channels were blocked with the use of intracellular injections of cesium. Input resistance ( R N), R ms/ R md, a conductance representing voltage-dependent potassium channels on the soma, G K, and a conductance attributed to damage caused by electrode impalement, G Da, were estimated from voltage responses to a step of current. The effect of intracellular injections of cesium on electrotonic structure was determined with the use of two strategies: 1) a population analysis that compared data from two groups of motoneurons, those recorded with potassium acetate electrodes (control group) and those recorded with cesium acetate electrodes after the motoneurons were loaded with cesium; and 2) an analysis of changes in electrotonic structure that occurred over the course of multiple injections of cesium or during similar periods of time in control cells. R N of control and cesium-loaded motoneurons was similar. Over the course of the recordings, R N of control cells usually increased and this increase was associated with a hyperpolarization. In contrast, increases in R N after successive injections of cesium were closely linked to a depolarization. At corresponding membrane potentials, R ms/ R md of cesium-loaded motoneurons was greater than R ms/ R md of control motoneurons. Over the course of cesium injections, R ms/ R md increased and the membrane potential depolarized. In contrast, increases in R ms/ R md observed during the course of recordings from control cells were associated with a hyperpolarization. Compared with control cells at corresponding membrane potentials, G K was less in cesium-loaded cells. Increases in G K that occurred over the course of recordings in control cells were closely coupled to a depolarization. In cesium-loaded cells, G K usually decreased as the cell depolarized during the injections. In control cells, increases in G Da that occurred during the recording period were closely coupled to a depolarization. In contrast, changes in G Da that occurred during cesium injections were not related to the change in membrane potential and did not explain the corresponding changes in R ms/ R md and membrane potential. The results of this study indicate that voltage-dependent potassium channels contribute to the somatic shunt (low R ms) in neck motoneurons and provide a voltage-dependent mechanism for the dynamic regulation of motoneuron electrotonic properties.

Vestibulospinal effects on neurons in different regions of the gray matter of the cat upper cervical cord

1. Previous studies of vestibular effects on the upper cervical cord have concentrated on the lateral and medial vestibulospinal tracts and on the actions that they exert on neck motoneurons and other neurons in the ventral horn. It is known, however, that both the rostral and the caudal areas of the vestibular nuclei (VN) give rise to axons that are located in the dorsal and dorsolateral funiculi and that terminate in the dorsal horn. A primary goal of our experiments was to investigate the effect of VN stimulation on neurons dorsal to lamina VII. 2. In decerebrate cats with the caudal cerebellar vermis removed, we stimulated different areas of the VN with an array of electrode. The area of stimulation extended from the caudal tip of the descending nucleus to Deiters' nucleus, and was divided into rostral and caudal halves with the use of the descending nucleus as a reference. For control purposes some stimulating points were placed in the external cuneate nucleus and restiform body. 3. We tested the effects of VN stimulation on spontaneously firing neurons in the ipsilateral C2 and C3 segments. For purposes of classification the gray matter was divided into four zones corresponding approximately to laminae 1-IV, V-VI, VII, and VIII of Rexed. Overall, the activity of 39 of 84 neurons was influenced from one or more stimulating sites. For six cells there was some possibility of current spread to the external cuneate nucleus or to the underlying reticular formation. 4. VN-evoked effects could consist of facilitation, or, less often, inhibition. In the majority of facilitated neurons conditioning stimuli evoked a synchronized, short-latency, increase in firing probability. When evoked by single stimuli this facilitation was considered monosynaptic. Facilitation that was diffuse, or that was only evoked by two or more stimuli, presumably involved more complex pathways. The latency of inhibition could not be measured, but was short. 5. Stimulation of either the rostral or caudal VN had no effect on neurons in laminae I-IV. Electrodes placed rostrally had little effect on neurons in laminae V-VI, but influenced more than half the neurons in laminae VII-VIII. Conversely, electrodes placed caudally were most effective on cells in laminae V-VII, although they also influenced some neurons in lamina VIII. 6. Stimulation of the dorsal rami influenced most neurons in laminae V-VI, and about a quarter of the neurons in laminae VII-VIII. When tested, there was often convergence between vestibulospinal and peripheral inputs. 7. Our results provide physiological evidence that vestibulospinal fibers influence neurons not only in laminae VII and VIII, but also as far dorsally as lamina V. Fibers that influence neurons in laminae V and VI originate primarily in the caudal areas of the VN. As suggested previously on anatomic grounds, the projection to the dorsal laminae, which is predominantly facilitatory, often converges with afferent input and can therefore modulate its influence on spinal neurons.

Trisynaptic inhibition from the contralateral vertical semicircular canal nerves to neck motoneurons mediated by spinal commissural neurons

1. Neck motoneurons usually receive disynaptic excitation and inhibition from individual semicircular canal nerves. However, in motoneurons of some neck muscles, trisynaptic inhibition is evoked by stimulation of the contralateral vertical canal nerves. The present study was performed to analyze this pathway and the location and properties of the last-order interneurons responsible for mediating this trisynaptic inhibition from the contralateral vertical canal nerves to neck motoneurons in anesthetized cats. 2. Bipolar stimulating electrodes were implanted on the contralateral anterior (ACN), lateral (LCN), and posterior canal nerve (PCN), and postsynaptic potentials (PSPs) evoked by electrical stimulation of individual canal nerves were intracellularly recorded from motoneurons of the obliquus capitis inferior (OCI), longus capitis (LC), and rectus capitis posterior (RCP) muscles. Stimulation of the contralateral ACN evoked trisynaptic inhibitory PSPs (IPSPs) in OCI and LC motoneurons and disynaptic excitatory PSPs (EPSPs) in RCP motoneurons. Stimulation of the contralateral PCN evoked di- and trisynaptic IPSPs in OCI and RCP motoneurons and disynaptic EPSPs in LC motoneurons. Stimulation of the contralateral LCN evoked disynaptic EPSPs in all of the motoneurons examined. 3. To determine the pathway that mediates these trisynaptic IPSPs from the vertical canal nerves to neck motoneurons, a lesion was made in the lower medulla, and the patterns of PSPs evoked by stimulation of the three contralateral canal nerves were compared before and after the lesion. Interruption of the ipsilateral medial longitudinal fascicle (MLF) abolished all disynaptic EPSPs and IPSPs from the three contralateral canal nerves in OCI, LC, and RCP motoneurons. In contrast, trisynaptic IPSPs evoked by stimulation of the contralateral ACN or PCN remained unaffected by sectioning the MLFs bilaterally. Sectioning of the contralateral lateral vestibulospinal tract (LVST) eliminated the trisynaptic IPSPs in OCI and LC motoneurons evoked by contralateral ACN stimulation and trisynaptic IPSPs in OCI and RCP motoneurons evoked by contralateral PCN stimulation but did not affect disynaptic EPSPs and IPSPs. 4. Stimulation of the contralateral LVST in the lower medulla after sectioning the bilateral MLFs evoked disynaptic IPSPs in OCI, LC, and RCP motoneurons. Because the LVST only projects ipsilaterally, this finding indicates that the last-order interneurons that mediate the trisynaptic inhibition through the LVST are most likely commissural neurons located in the spinal cord. 5. To determine the locations of last-order commissural neurons terminating on OCI motoneurons, wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) was injected into the OCI muscle nerve at C1.(ABSTRACT TRUNCATED AT 400 WORDS)

Innervation of motoneurons based on dendritic orientation

1. The distribution of terminals from vestibulospinal (VS) axons on the dendritic trees of neck motoneurons was determined by combining the anterograde transport of Phaseolus Vulgaris Leucoagglutinin (PHA-L) with intracellular staining techniques and three-dimensional reconstruction methods. 2. Contacts between VS axon terminals and dendrites were arranged in a nonuniform pattern that depended on the orientation (i.e., rostro-caudal vs. dorsolateral) of the dendrites. 3. This innervation pattern satisfies a critical structural condition necessary for selective nonlinear interactions between pairs of simultaneously active inputs to motoneurons.