Neck Motoneurons Research Articles

Innervation of multiple neck motor nuclei by single reticulospinal tract axons receiving tectal input in the upper cervical spinal cord

Axons of reticulospinal neurons (RSNs) activated monosynaptically by stimulation of the contralateral superior colliculus (SC) were stained with intraaxonal injection of horseradish peroxidase in the cat upper cervical spinal cord. Stem axons of single RSNs gave rise to multiple axon collaterals to laminae IX, VIII and VII over a few cervical segments. Single RSNs made contacts with retrogradely labeled neck motoneurons of different neck muscles. Therefore, RSNs were regarded as mediating output of the SC to functionally different groups of neck muscles simultaneously. The result gave evidence of neural implementation of a functional synergy for a neck movement at a single neuron level.

Connections between utricular nerve and neck flexor motoneurons of decerebrate cats.

We studied the circuitry between the utricular (UT) nerve and ventral neck motoneurons innervating the longus capitis (LC), a neck flexor muscle, in decerebrate cats. We recorded intracellularly from 63 LC (ipsilateral 37, contralateral 26) motoneurons in C1 and C2 segments. UT nerve stimulation evoked disynaptic, excitatory postsynaptic potentials in all ipsilateral LC motoneurons, and inhibitory postsynaptic potentials that were at least trisynaptic in almost all contralateral LC motoneurons. UT effects on neck motoneurons innervating muscles involved in flexion and lateral turning are similar to the connections between the UT nerve and neck extensor motoneurons. These neuron circuits may play a role in fixing the head and the neck to the body during horizontal linear acceleration.

Response of commissural and other upper cervical ventral horn neurons to vestibular stimuli in vertical planes.

1. To study their contribution to the vestibulocollic reflex, we have studied, in decerebrate paralyzed cats, the effect of sinusoidal vestibular stimulation in multiple vertical planes on the spontaneous activity of neurons in the C3 ventral horn. Antidromic microstimulation was used to identify 17/42 neurons as commissural; 10 of these were confirmed to have a projection to the contralateral ventral horn. 2. Dynamics of the responses of spontaneously firing neurons were studied with 0.05-1 Hz sinusoidal stimuli delivered near the plane of rotation that produced maximal modulation of neuron activity (response vector orientation). On the basis of their responses, we classified 38 neurons as receiving otolith, semicircular canal, or otolith + canal input. All three response types were found among commissure and nonantidromic neurons. 3. Two-thirds of neuron response vector orientations pointed contralaterally. They were either near the anterior or posterior canal planes or in the roll quadrant. In the case of neurons with input from canals, the latter indicates convergence from the vertical canals on the same side. There were almost no vectors in the pitch quadrants. The distribution of response vector orientations resembles that seen in the vestibular nuclei and pontomedullary reticular formation, suggesting that commissural neurons may not make a new contribution to spatial processing in the vertical vestibulocollic reflex. 4. It is presumed that commissural neurons are premotor. If so, some have the properties to be in the pathway between the contralateral utricle and neck motoneurons. More generally, their actions could modify the effectiveness of vestibulospinal and reticulospinal fibers that have similar spatial properties and make synapses with neck motoneurons.

Succular effects on neck motoneurons in the decerebrate cats

Succular effects on neck motoneurons in the decerebrate cats

Facial input to neck motoneurons: trigemino-cervical reflexes in the conscious and anaesthetised cat.

Cutaneous facial inputs influencing head movement were examined in the conscious and anaesthetised cat. EMG recordings were made in neck muscles of conscious, unrestrained cats in which an unexpected light cutaneous stimulus was applied to the glabrous skin of the planum nasale (PN). These observations established that head aversion movements were associated with synchronised activation of both deep and superficial dorsal neck muscles. In anaesthetised cats in which activity in the motoneurons of the large dorsal neck muscles was examined, mechanical stimulation of the PN or electrical stimulation of the infraorbital nerve (ION) produced a short latency, reflex activation. The reflex could be elicited by excitation of low threshold, rapidly conducting fibres in the ION. Intracellular recording from neck motoneurons showed that there is a short latency, probably disynaptic, excitatory pathway from low threshold nerves in the ION to neck motoneurons, but discharge of neck motoneurons occurred several milliseconds later, presumably as a result of activity in a longer multisynaptic pathway.

Effects of cerebral neuron C-PR on body postural muscles associated with a food-induced arousal state in Aplysia

1. Firing of cerebral neuron, C-PR, produced complex bilateral movements of various regions of the body of the marine mollusc Aplysia californica. The movements were similar to those seen when the animal assumes the head-up feeding posture during food-induced arousal. Muscles of the neck largely contracted in transverse and longitudinal directions, and large transverse movements were also induced in the middle part of the foot. On the other hand, firing of C-PR appeared to relax the anterior part of the foot in transverse and longitudinal directions. 2. We identified pedal-ganglion motor neurons that innervate various regions of the animal, and explored the synaptic connections of C-PR with these neurons. Firing of C-PR produced synaptic potentials bilaterally in most of the identified motor neurons. 3. Motor neurons for the neck were largely excited by C-PR firing. C-PR firing also excited the motor neurons that produce transverse movements of the middle part of the foot. On the other hand, C-PR inhibited the spontaneous spike activity of the motor neurons for the anterior part of the foot. 4. One neck motor neuron was found to receive a monosynaptic excitatory postsynaptic potential (EPSP) from C-PR, but the postsynaptic potentials (PSPs) induced by C-PR in the other identified motor neurons were mediated polysynaptically. 5. We also found that the C-PR can modulate movements evoked by firing of the motor neurons for the ipsilateral neck and anterior foot. C-PR enhanced both transverse and longitudinal contractions of the neck. 6. For the anterior foot region, C-PR had different modulatory effects on the longitudinal and the transverse contractions. C-PR largely enhanced or initially depressed and then enhanced longitudinal contractions, whereas C-PR depressed transverse contractions. 7. The overall results support the hypothesis that C-PR is involved in controlling the head-up posture when the animal is aroused by food.

1510 Inhibitory commissural neurons in laminae VII and VIII mediating trisynaptic inhibition from the contralateral vertical ampullary nerves to neck motoneurons

1510 Inhibitory commissural neurons in laminae VII and VIII mediating trisynaptic inhibition from the contralateral vertical ampullary nerves to neck motoneurons

Chapter 19 Synaptic organization of the vestibulo-collic pathways from six semicircular canals to motoneurons of different neck muscles

The pattern of inputs from six semicircular canals to neck motoneurons was investigated by stimulating six ampullary nerves electrically and recording intracellular potentials from motoneurons of the rectus capitis dorsalis (RD), the complexus (COMP) and the obliquus capitis caudalis (OCA) muscles at the upper cervical cord of the cat. RD and COMP motoneurons received disynaptic excitation from bilateral anterior and contralateral horizontal ampullary nerves and disynaptic inhibition from bilateral posterior and ipsilateral horizontal ampullary nerves. OCA motoneurons received excitation from ipsilateral vertical and contralateral horizontal ampullary nerves and inhibition from contralateral vertical and ipsilateral horizontal ampullary nerves. Ipsilateral disynaptic inhibitory postsynaptic potentials and contralateral disynaptic excitatory postsynaptic potentials to these motoneurons were mediated by the medial longitudinal fasciculus (MLF) and the other postsynaptic potentials by the extra-MLF pathways. The results indicated that motoneurons of a neck muscle have its own characteristic pattern of inputs from six semicircular canals.

Trigeminal excitation of dorsal neck motoneurones in the cat.

Excitation of dorsal neck motoneurones evoked by electrical stimulation of primary trigeminal afferents in the Gasserian ganglion has been investigated with intracellular recording from alpha-motoneurones in the cat. Single stimulation in the Gasserian ganglion ipsi- and contralateral to the recording side evoked excitatory postsynaptic potentials (EPSPs) in motoneurones innervating the lateral head flexor muscle splenius (SPL) and the head elevator muscles biventer cervicis and complexus (BCC). The gasserian EPSPs were composed of early and late components which gave the EPSPs a hump-like shape. A short train of stimuli, consisting of two to three volleys, evoked temporal facilitation of both the early and late EPSP components. The latencies of the gasserian EPSPs ranged from 1.6 to 3.6 ms in SPL motoneurones and from 1.6 to 5.8 ms among BCC motoneurones. A rather similar latency distribution between 1.6 and 2.4 ms was found for ipsi- and contralateral EPSPs in SPL and BCC motoneurones, which is compatible with a minimal disynaptic linkage between primary trigeminal afferents and neck motoneurones. Systematic transections of the ipsi- and contralateral trigeminal tracts were performed in the brain stem between 3 and 12 mm rostral to the level of obex. The results demonstrate that both the ipsi- and contralateral disynaptic and late gasserian EPSPs can be mediated via trigeminospinal neurones which take their origin in the nucleus trigeminalis spinalis oralis. Transection of the midline showed that the contralateral trigeminospinal neurones cross in the brain stem. Systematic tracking in and around the ipsilateral trigeminal nuclei demonstrated that the axons of ipsilateral trigeminospinal neurones descend just medial to and/or in the medial part of the nucleus. Spinal cord lesions revealed a location of the axons of the ipsilateral trigeminospinal neurones in the lateral and ventral funiculi. Interaction between the ipsi- and contralateral gasserian EPSPs showed complete summation of the disynaptic EPSP component, while the late components were occluded by about 45%. These results show that the disynaptic EPSPs are mediated by separate trigeminospinal neurones from the ipsi- and contralateral side, while about half of the late EPSPs are mediated by common neurones which receive strong bilateral excitation from commissural neurones in the trigeminal nuclei. Spatial facilitation was found in the late gasserian EPSP but not in the disynaptic gasserian EPSP by conditioning stimulation of cortico- and tectofugal fibres. Disynaptic pyramidal and tectal EPSPs, which are mediated by reticulospinal neurones, were facilitated by a single stimulation in the gasserian ganglion at an optimal interval of 2 ms.(ABSTRACT TRUNCATED AT 400 WORDS)

Spinal commissural neurons mediating vestibular input to neck motoneurons in the cat upper cervical spinal cord

Spinal commissural neurons (CNs) activated di- or trisynaptically by stimulation of ipsilateral vestibular afferents were stained with intraaxonal injection of horseradish peroxidase in the cat upper cervical spinal cord. Stem axons of CNs in lamina VIII or VII, after crossing the midline, had ascending and/or descending main branches that gave off multiple axon collaterals to laminae IX and VIII over a few cervical segments. Terminal boutons appeared to make contact with proximal dendrites and somata of retrogradely-labelled neck motoneurons. Therefore, these CNs were regarded as mediating vestibular afferent input to contralateral neck motoneurons trisynaptically at the shortest.

Descending pathways mediating disynaptic excitation of dorsal neck motoneurones in the cat: facilitatory interactions

Facilitatory interactions between disynaptic EPSPs evoked from the contralateral tectum, ipsilateral tegmentum and contra- and/or ipsilateral pyramid have been investigated in dorsal neck motoneurones of the cat. Monosynaptic convergence on common intercalated neurones was found from ipsi- and contralateral pyramidal, contralateral tectal and ipsilateral tegmental fibres. In addition, disynaptic facilitation was observed from ipsilateral pyramidal fibres on disynaptic contralateral pyramidal EPSPs. Transection of cortico-fugal fibres in the pyramid showed that the location of the interactions occurred in the lower brain stem, suggesting that reticulospinal neurones are mediating the effects.

Descending pathways mediating disynaptic excitation of dorsal neck motoneurones in the cat: brain stem relay

The location of intercalated neurones mediating disynaptic excitation from tectum, tegmentum and pyramids to dorsal neck motoneurones has been investigated by: (a) recording field potentials in the lower brain stem evoked from the above systems, (b) systematic stimulation in the brain stem during intracellular recording from motoneurones innervating the splenius, biventer cervicis and complexus muscles, and (c) comparing the effects of lesions of the brain stem with kainic acid on the disynaptic EPSPs elicited from the above three systems. Electrical stimulation of the contralateral superior colliculus evoked monosynaptic field potentials which were largest in the caudal pontine reticular formation rostral to the abducens nucleus and in the rostral part of the medullary reticular formation caudal to the abducens nucleus. Likewise, stimulation of the ipsilateral tegmentum (the cuneiform and subcuneiform nucleus) evoked field potentials which were large in the caudal medulla and small in the pons. In contrast, stimulation of the contralateral tegmentum was ineffective in evoking field potentials. Stimulation of the pyramid 2–3 mm rostral to the obex elicited monosynaptic field potentials in the reticular formation of the lower brain stem that were only about 25% of those from the superior colliculus. In contrast to the field potentials from the superior colliculus, the pyramidal ones were large in the medulla and small in the pons. Lesions of the reticular formation in the lower brain stem by unilateral kainic acid injection caused disappearance of disynaptic EPSPs in motoneurones from the above three systems. These results strongly suggest that the intercalated neurones mediating pyramidal, tectal and tegmental EPSPs are reticulospinal neurones in the lower brain stem. Systematic stimulation in various locations of the lower brain stem showed that monosynaptic EPSPs were evoked from the regions of the reticular formation which received projection from the above three descending systems. The effective regions for evoking the EPSPs in splenius (SPL) were located somewhat more dorsally than for biventer cervicis and complexus (BCC) motoneurones. The descending axons of presumed reticulospinal neurones were stimulated with electrodes placed in medial, middle and lateral positions at the spinomedullary junction. Monosynaptic EPSPs in SPL and BCC motoneurones were evoked from the medial and middle electrodes but not from the lateral electrode.

Tectal and tegmental excitation in dorsal neck motoneurones of the cat.

1. Intracellular recordings were made from 116 splenius (SPL) and 103 biventer cervicis and complexus (BCC) alpha-motoneurones in nineteen cats anaesthetized with alpha-chloralose. 2. Electrical stimulation in the contralateral tectum evoked disynaptic excitatory postsynaptic potentials (EPSPs) in the motoneurones when a train of stimuli was applied in the ventral layers throughout the superior colliculus. In the rostral half of the superior colliculus, these EPSPs were due to stimulation of ascending collaterals of tectofugal neurones. EPSPs of a presumed trisynaptic linkage could only be evoked from the dorsal and intermediate tectal layers in the caudal half of the superior colliculus. It is concluded that the tectofugal neurones which evoked the disynaptic EPSPs are mainly located in the caudal half of the superior colliculus. 3. Disynaptic EPSPs were evoked in the motoneurones by a train of stimuli in the contralateral fields of Forel and Zona incerta, which were due to stimulation of ascending collaterals from the tectofugal neurones. 4. Spatial facilitation experiments revealed that tectal disynaptic EPSPs in the neck motoneurones were mediated via reticulospinal neurones with convergent input from cortico-reticular neurones. 5. A train of stimuli in the ipsilateral tectum evoked EPSPs with latencies compatible with a trisynaptic linkage, while disynaptic EPSPs at low threshold could be elicited from the underlying tegmentum. Similar disynaptic EPSPs could be evoked from the ipsilateral fields of Forel. It is suggested that some of the disynaptic tegmental EPSPs in SPL and BCC motoneurones can be mediated via a tegmento-reticulospinal pathway which originates in the cuneiform nucleus.

Connections from the lateral vestibular nucleus to the upper cervical spinal cord of the cat: a study with the anterograde tracer PHA-L.

The projections of neurons in the lateral vestibular nucleus (LVN) to the upper cervical spinal cord of the cat were investigated by means of the anterograde tracer Phaseolus vulgaris leucoagglutinin (PHA-L). At the junction of C1 and C2, axons were distributed bilaterally in the ventromedial funiculi, and ipsilaterally in the ventrolateral and lateral funiculi. The majority of boutons were found ipsilateral to the injection sites and most of these boutons were found at the base of the ventral horn and throughout the medial two-thirds of lamina VIII. A more modest termination zone was found along the ventral border of lamina VII and a small number of boutons were scattered in the dorsal horn. Contralateral termination zones were similar to the ipsilateral projections. There were significant changes in the distribution of vestibulospinal axons and density of boutons at the junction of C3 and C4. At this level, most vestibulospinal axons travelled ipsilaterally and were found along the medial border of the ventromedial funiculus and the ventral margin of the ventrolateral funiculus. The overall distribution of boutons near the border of C3 and C4 was similar to the pattern seen at the junction of C1 and C2. However, bouton density fell by a factor of three. Large zones of the grey matter were devoid of boutons in individual experiments. These results demonstrate that the projections of neurons in the LVN to the upper cervical spinal cord are densest in the regions containing motoneurons supplying suboccipital muscles. This result suggests that monosynaptic connections to those motoneurons may be an important part of the neural circuitry responsible for vestibulocollic reflexes. However, the large number of boutons found in regions dorsal to motoneuron nuclei in all upper cervical segments indicates that the primary path from vestibulospinal axons to neck motoneurons may be indirect and involve relays via spinal interneurons.

Connections between utricular nerve and dorsal neck motoneurons of the decerebrate cat.

1. We studied connections between the utricular (UT) nerve and dorsal neck motoneurons in decerebrate cats. Electrodes were fixed in place on the UT nerve under visual observation; the other branches of the vestibular nerve were transected. 2. The N1 field potential evoked by UT nerve stimulation was recorded in the vestibular nuclei at the start of each experiment. The potential typically grew until it reached a plateau. Stimulus spread (if any) to the central ends of other nerve branches was revealed by an additional increase in N1 amplitude after the plateau was reached. 3. We recorded intracellularly from 55 motoneurons in C1-C3. Some were identified as having axons in the dorsal rami, which innervate dorsal neck muscles. Others projected in nerves that were not available for stimulation. 4. UT nerve stimulation evoked synaptic potentials in essentially all motoneurons studied. The predominant pattern consisted of disynaptic excitatory postsynaptic potentials in ipsilateral motoneurons and inhibitory postsynaptic potentials that were at least trisynaptic in contralateral motoneurons. 5. The results demonstrate the presence of short-latency connections between the utricular nerve and dorsal neck motoneurons. The functional role of this pathway remains to be investigated.

Patterns of connections between six semicircular canals and neck motoneurons.

Patterns of connections between six semicircular canals and neck motoneurons.

Mono- and disynaptic pathways from Forel's field H to dorsal neck motoneurones in the cat.

1. We analysed the synaptic actions produced by Forel's field H (FFH) neurones on dorsal neck motoneurones and the pathways mediating the effects. 2. Stimulation of ipsilateral FFH induced negative field potentials of several hundred microvolts with the latency of about 1.1 ms in the medial ponto-medullary reticular formation, being largest in the ventral part of the nucleus reticularis pontis caudalis (NRPC), and in the dorsal part of the nucleus reticularis gigantocellularis (NRG). 3. Stimulation of ipsilateral FFH induced excitatory postsynaptic potentials (EPSPs) in 90% (47/52) and inhibitory postsynaptic potentials (IPSPs) in 19% (10/52) of the reticulospinal neurones (RSNs) in the NRPC and the NRG. Latencies of the EPSPs and IPSPs were 0.7-3.0 ms, the majority of which were in the monosynaptic range. The monosynaptic connexions were confirmed by spike triggered averaging technique both in excitatory (n = 4) and inhibitory (n = 2) pathways. 4. Single stimulation of FFH induced EPSPs at the segmental latencies of 0.3-1.0 ms in neck motoneurones, which were clearly in the monosynaptic range. Repetitive stimulation of FFH produced marked temporal facilitation of EPSPs in neck motoneurones. The facilitated components of the EPSPs had a little longer latencies and their amplitude reached several times as large as that evoked by single stimulation in all the tested motoneurones. These facilitated excitations are assumed to be mediated by RSNs in the NRPC and NRG, since RSNs were mono- and polysynaptically fired by stimulation of FFH and they were previously shown to directly project to neck motoneurones. 5. EPSPs were induced in 91% (82/91) of motoneurones supplying m. biventer cervicis and complexus (BCC; head elevator), 10% (3/29) of motoneurones supplying m. splenius (SPL; lateral head flexor). Likewise, stimulation of FFH produced EMG responses in BCC muscles, while not in SPL muscle. Thus FFH neurones produce excitations preferentially in BCC motoneurones. 6. Systematic tracking in and around FFH revealed that the effective sites for evoking above effects were in FFH and extended caudally along their efferent axonal course. 7. These results suggested that FFH neurones connect with neck motoneurones (chiefly BCC, head elevator) mono-, di- and/or polysynaptically and are mainly concerned with the control of vertical head movements.

Projections of the tectospinal tract to the upper cervical spinal cord of the cat: A study with the anterograde tracer PHA‐L

The goal of the present experiments was to re-examine the spinal projections of neurons in the superior colliculus (SC) of the cat by taking advantage of the high sensitivity of the anterograde tracer, phaseolus vulgaris leucoagglutinin (PHA-L). In seven experiments, multiple injections of PHA-L into different regions of the SC labelled a total of 172 axons in the predorsal bundle; yet only 11 tectospinal tract (TST) axons were found in the upper cervical spinal cord. Collaterals emerging from these axons were rare and arose exclusively from TST axons with a diameter of less than 1 micron. Individual collaterals had different termination zones: some terminated in the lateral part of lamina V and VI after taking a dorsolateral course through lamina VII and VIII; others terminated in the medial part of lamina VII. One collateral terminated within lamina IX and the ventral part of lamina VIII. The combined termination of all collaterals was densest in lamina VII and dorsal lamina VIII. A small number of boutons were also found in the lateral parts of laminae V and VI, and in lamina IX and immediately adjacent regions in lamina VIII. Compared to axons belonging to other spinal descending systems, individual TST axons give rise to much simpler intraspinal collaterals with relatively few boutons. This feature, together with the relative paucity of TST axons, suggests that direct connections from the SC to neurons in the upper cervical spinal cord are sparse. Furthermore, our results are consistent with electrophysiological studies that show that few, if any, neck motoneurons receive monosynaptic connections from TST neurons. Projections to neck motoneurons must therefore involve a relay, either through other descending pathways, such as the reticulospinal system, or via local segmental interneurons.

The neuronal organization of horizontal semicircular canalactivated inhibitory vestibulocollic neurons in the cat

1. The somatic location and axonal projections of inhibitory vestibular nucleus neurons activated by the horizontal semicircular canal nerve (HCN) were studied in anesthetized cats. Cats were anesthetized with ketamine hydrochloride and pentobarbital sodium. 2. Intracellular recordings were obtained from 11 neck extensor motoneurons which were identified by antidromic activation from the dosal rami (DR) in the C1 segment. Stimulation of the ipsilateral (i-) HCN and the ipsilateral abducens (AB) nucleus evoked IPSPs in the motoneurons. These IPSPs were fully or partially occluded when they were evoked simultaneously. 3. Intracellular recordings were obtained from 8 AB motoneurons. Stimulation of the i-HCN and the i-C1DR motoneuron pool evoked IPSPs in the AB motoneurons. These IPSPs were also partially occluded when they were evoked simultaneously, which implied that some HCN-activated neurons inhibit both i-AB motoneurons and ipsilateral neck motoneurons. 4. Unit activity was extracellularly recorded from 30 vestibular neurons that were activated monosynaptically by i-HCN stimulation. Their axonal projections were determined by stimulating the i-AB nucleus and the i-C1DR motoneuron pool. Eight neurons were activated by both stimuli, and were termed vestibulooculo-collic (VOC) neurons. Their axonal branching was examined by means of local stimulation in and around the i-AB nucleus and the i-C1DR motoneuron pool. Eighteen neurons were antidromically activated from the i-C1DR motoneuron pool but not from the i-AB nucleus. These were termed vestibulo-collic (VC) neurons. Four neurons were activated from the i-AB nucleus but not from the ventral funiculus in the C1 segment, and were termed vestibulo-ocular (VO) neurons.(ABSTRACT TRUNCATED AT 250 WORDS)

Active zone organization and vesicle content scale with bouton size at a vertebrate central synapse

A common observation in studies of neuronal structure is that axons differ in the size of their synaptic boutons. The significance of this size variation is unclear, in part because we do not know how the size of synaptic boutons is related to their internal organization. The present study has addressed this issue by using three-dimensional reconstruction of serial thin sections to examine the ultrastructure of synaptic boutons that vary in size. Our observations are based on complete or near-complete reconstructions of 53 synaptic boutons contacting large neurons in the ventromedial gray matter of the upper cervical spinal cord (probable neck motor neurons). We characterized bouton size in terms of volume and total area of membrane apposed to the motor neuron surface (apposition area). Boutons vary in apposition area by a factor of 40, and there is a significant positive correlation between our two measures of bouton size. In addition, bouton size is systematically related to four ultrastructural variables: 1) total active zone area, 2) number of active zones, 3) individual active zone area, and 4) number of synaptic vesicles. The correlations between these variables and both of our measures of bouton size are positive and significant. These data suggest that bouton size may be an index of ultrastructural features that are thought to influence transmitter storage and release.