B. W. Peterson

Patterns of projection and branching of reticulospinal neurons

SummaryExtracellular microelectrodes were used to record the activity of reticulospinal neurons within the medial ponto-medullary reticular formation in the cat. In one series of experiments reticulospinal neurons were activated from electrodes in the ventro-medial reticulospinal tract (RSTm) and in the ipsiand contralateral lateral reticulospinal tracts (RSTi, RSTC) at spinal levels C1–2, C4, Th1 and L1. RSTm neurons were found primarily in n.r. pontis caudalis and the rostro-dorsal part of n.r. gigantocellularis. 71% of these neurons projected as far as the lumbar spinal cord. RSTi neurons projecting to C4 and beyond were clustered in the caudo-ventral part of n.r. gigantocellularis, but those RSTi neurons projecting to the first three cervical segments were located more rostro-dorsally. In all, 63% of the RSTi neurons projected to the lumbar spinal cord. RSTc neurons, which comprised only 5% of the reticulospinal population, were found throughout n.r. gigantocellularis. RSTm neurons had a median conduction velocity of 101 m/sec whereas RSTi and RSTc had median conduction velocities on the order of 70 m/sec.In a second series of experiments microstimulation was used to activate branches of reticulospinal neurons within the gray matter of the cervical enlargement. Twenty-two of thirty-three neurons found to project to the cervical ventral horn were branching neurons that also sent axons to the lumbar spinal cord. Thus much of the reticulospinal activity reaching the cervical enlargement also acts at one or more other spinal levels. Detailed investigation of the course of reticulospinal axons within the cervical gray matter indicated that a single axon may traverse wide areas of the ventral horn including regions on both sides of the spinal cord.

Reticulospinal connections with limb and axial motoneurons.

SummaryResponses of motoneurons supplying muscles of the forelimbs, hindlimbs, back, and neck to stimulation of the medial pontomedullary reticular formation were studied with intracellular recording in cere-bellectomized cats under chloralose anesthesia.Stimulation of the midline or of a reticular region consisting of nucleus reticularis (n.r.) pontis caudalis and the dorsorostral part of n.r. gigantocellularis produced monosynaptic excitation of ipsilateral motoneurons supplying axial muscles and flexor and extensor muscles in both proximal and distal parts of the limbs. This widespread excitation appears to have been produced by rapidly conducting medial reticulospinal fibers.Stimulation of a second region consisting of n.r. ventralis and the ventrocaudal part of n. r. gigantocellularis produced monosynaptic excitation of ipsilateral neck and back motoneurons but only longer latency, apparently multisynaptic excitation of limb motoneurons. Collision tests indicated that this monosynaptic excitation did not involve fibers descending along the midline. It therefore appears to have been produced by lateral reticulospinal fibers.Reticular stimulation also produced short latency, monosynaptic inhibition of neck motoneurons, long latency, apparently polysynaptic inhibition of limb motoneurons and intermediate latency inhibition of back motoneurons. The latencies and properties of inhibitory responses of back motoneurons indicated that they were produced either disynaptically by fast fibers or monosynaptically by slower fibers.The data indicate that the medial pontomedullary reticular formation can be divided into a number of different zones each with a distinct pattern of connections with somatic motoneurons. These include the dorsorostrally located medial reticulospinal projection area, from which direct excitation of a wide variety of motoneurons can be evoked, the ventrocaudally located lateral reticulospinal projection area from which direct excitation of neck and back and direct inhibition of neck motoneurons can be evoked and the dorsal strip of n.r. gigantocellularis which has direct excitatory and inhibitory actions only on neck motoneurons.

Reticulospinal excitation and inhibition of neck motoneurons

SummaryResponses of neck motoneurons to electrical stimulation of the pontomedullary reticular formation were recorded intracellularly in cerebellectomized cats anesthetized with chloralose. Stimulation of nucleus reticularis (n.r.) ventralis and the dorsal part of n.r. gigantocellularis evoked short latency, monosynaptic inhibitory postsynaptic potentials (IPSPs) in the majority of motoneurons supplying the ipsilateral splenius, biventer cervicis and complexus muscles and in 25% of motoneurons projecting in the ipsilateral spinal accessory nerve. Monosynaptic IPSPs were also evoked by stimulating the medial longitudinal fasciculus (MLF) but lesion and collision experiments indicated that these IPSPs were independent of those evoked by reticular stimulation. Monosynaptic IPSPs were also occasionally observed following stimulation of the contralateral reticular formation, especially of the dorsal part of n.r. gigantocellularis.Monosynaptic excitatory postsynaptic potentials (EPSPs) were evoked in all classes of neck motoneurons studied by stimulation of n.r. pontis caudalis, gigantocellularis and ventralis. Each reticular nucleus appeared to contribute to this excitation. The excitation was bilateral but large monosynaptic EPSPs were most often seen in motoneurons ipsilateral to the stimulus site. Data indicated that pontine EPSPs were mediated by ventromedial reticulospinal fibers while medullary EPSPs were mediated by ventrolateral reticulospinal fibers. Neck motoneurons thus receive at least three distinct direct reticulospinal inputs, two excitatory and one inhibitory.

Cat spinoreticular neurons: Locations, responses and changes in responses during repetitive stimulation

Neurons in the lumbosacral spinal cord which project to the medial pontomedulary reticular formation were studied in the chloralose-anesthetized cat. Such neurons, identified by antidromic activation, were found predominantly in lamina VIII and medial lamina VII, and most were found to project to the contralateral reticular formation. Receptive fields for natural stimuli were generally complex, having various combinations of excitatory and inhibitory areas ipsi- and/or contralaterally. Adequate stimuli ranged from innocuous to noxious, with the stimuli required for decreasing a neurons activity usually more intense than the stimulus required for increasing it. Electrical stimulation of hindlimb nerves indicated the presence of extensive convergence. Responses of spinoreticular neurons were found to decline during periods of repetitive stimulation. The response decrements were found to have many of the parametric features of behavioral habituation and were similar to response decrements previously observed in the medial pontomedullary reticular formation.

Dynamic properties of vestibular reflexes in the decerebrate cat

SummaryVestibulocollic (VCR) and vestibulo-ocular (VOR) reflexes were studied during angular rotation in the horizontal plane in precollicular decerebrate cats. Angular position was modulated by sinusoids or sums of sinusoids with frequencies ranging from 0.05 to 5 Hz.Reflex motor output was measured by recording electromyographic (EMG) activity of the lateral rectus and dorsal neck muscles and discharge of abducens motoneurons. Measured with respect to input angular acceleration VCR motor output displayed a second order lag at low frequencies, bringing mean EMG phase (−136 °) and gain slope (−35 dB/ decade) close to those of an angular position signal at 0.2 Hz. At higher frequencies the lag was counteracted by a second order lead bringing mean phase (−52 °) and gain slope (−5.6 dB/decade) back close to those of an angular acceleration signal at 3 Hz. By contrast, mean phase (−113 ° to −105 °) and gain slope (−21 to −28 dB/decade) of the VOR motor output remained close to those of an angular velocity signal across the entire frequency range.The data suggest that neural pathways producing the VCR receive selective input from “irregular type” horizontal semicircular canal afferents which provide one lag and one lead in the overall transfer function while the other lag and lead are produced by central pathways.Transaction of the medial longitudinal fasciculus (MLF), which eliminates all of the most direct (three neuron) arcs of the horizontal VCR, did not cause any detectable change in the horizontal VCR at either low or high frequencies. Reductions in overall gain occurred in some cases but these could be attributed to damage to axons outside the MLF. Less direct pathways, probably including vestibulo-reticulospinal pathways, are thus able to produce both the low-frequency, phase-lagging and high-frequency, phase-leading components of the horizontal VCR.

Vestibulospinal, reticulospinal and interstitiospinal pathways in the cat.

Publisher Summary This chapter reviews the properties and motor actions of three descending systems: the vestibulospinal tracts, the reticulospinal tracts, and the interstitiospinal tract. The vestibulospinal tracts are the most direct pathways between the labyrinth and spinal motoneurons. The medial vestibulospinal tract (MVST) is the predominant direct pathway to axial motoneurons, the lateral vestibulospinal tract (LVST) the only direct pathway to limb motoneurons; not much is known about the recently discovered caudal vestibulospinal tract. The role of these direct pathways in functionally meaningful vestibulospinal reflexes remains to be determined. The reticulospinal tracts consist of three groups of descending fibers: one descending in the ventromedial funiculus (RST m ), one in the ipsilateral ventrolateral funiculus (RST i ), and one in the contralateral ventrolateral funiculus (RST c ). Excitatory RST m neurons scattered throughout nucleus reticularis (n.r.) pontis candalis and the dorsal part of n.r. gigantocellularis establish direct synaptic connections with motoneurons supplying a wide variety of muscles throughout the body. The reticulospinal systems receive major direct inputs from many different regions including vestibular nuclei, suggesting that they participate in vestibulospinal reflexes. The interstitiospinal tract, which has not been studied extensively, includes neurons that establish direct excitatory connections with neck motoneurons, but do not establish direct connections with limb and back motoneurons.

Direct excitation of neck motoneurons by interstitiospinal fibers

Summary1.Responses of neck motoneurons to stimulation of the interstitial nucleus of Cajal (INC) were recorded intracellularly in cats under chloralose anesthesia. When stimuli were applied within or close to the INC, short latency, monosynaptic excitatory postsynaptic potentials (EPSPs) were evoked in many neck motoneurons. Such EPSPs were not evoked by stimulating mesencephalic regions outside the INC.2.Stimulation of the ipsilateral INC produced monosynaptic EPSPs consistently in biventer cervicis-complexus (BCC) motoneurons, while such EPSPs were observed in about two thirds of the splenius (SP) motoneurons and half of the trapezius (TR) motoneurons tested. Stimulation of the contralateral INC produced weak monosynaptic EPSPs in about half the BCC motoneurons and in a few SP and TR motoneurons. All types of motoneurons also received longer latency, apparently polysynaptic, PSPs from both INCs. In BCC and TR motoneurons these were mainly EPSPs, in SP, mixed excitatory and inhibitory PSPs.3.Monosynaptic EPSPs evoked by INC stimulation were not eliminated by acute and chronic parasagittal and transverse lesions placed to interrupt the bifurcating axons of all vestibulospinal and many reticulospinal neurons. No significant collision was observed between EPSPs evoked by INC and vestibular or reticular stimulation. The EPSPs evoked by stimulation of the INC therefore appear to have been produced by activation of interstitiospinal neurons rather than by an axon reflex mechanism.4.The properties of a number of interstitiospinal neurons were observed while recording extracellularly from the mesencephalon to map the location of the INC. One third of the interstitiospinal neurons activated antidromically from the C4 segment could also be activated antidromically from L1. These lumbar-projecting neurons had conduction velocities ranging from 15–123 m/s. Several interstitiospinal neurons sending axons to the ventral horn of the neck segments were identified and two of these were found to be branching neurons that projected both to the neck and to lower levels of the spinal cord.

Responses of medial reticular neurons to stimulation of the vestibular nerve

SummaryResponses of neurons in the medial ponto-medullary reticular formation to stimulation of vestibular nerves, bilateral pericruciate cortex and several cutaneous points were studied in cerebellectomized cats under chloralose-urethan or pentobarbital anesthesia. Reticulospinal neurons were identified by their antidromic responses to stimulation of cervical or lumbar spinal cord.Stimulation of the vestibular nerves with trains of three shocks evoked firing of approximately one third of the reticular neurons studied with extracellular recording. The same stimuli produced EPSPs or IPSPs in approximately 75% of the neurons studied with intracellular recording. Stimulus intensities required to evoke firing or PSPs ranged from 1.0 to over 10 times the threshold intensity for evoking a vestibular N1 potential.The shortest latency vestibular-evoked PSPs had properties which suggested that they were produced by a disynaptic pathway. Neurons receiving such short latency IPSPs were concentrated in the dorso-rostral part of n.r. gigantocellularis; neurons receiving short latency EPSPs were scattered throughout this nucleus, but were seldom found in the pontine reticular formation. Reticulospinal neurons were observed to receive short latency EPSPs but not short latency IPSPs.Reticular neurons often received convergent input from vestibular nerves, pericruciate cortex and several cutaneous points. No relationship was detected between such different inputs, but neurons tended to respond in a similar way to stimulation of both vestibular nerves, or of both pericruciate cortices or of different cutaneous points.

Direct fastigiospinal fibers in the cat

Projections o f the fastigial nucleus to the vestibular nuclear complex 6,8, the pontomedul lary reticular format ion 6,9 and the ventral thalamic complex1,3, 6 are well known. In 1956, Thomas et al. 6 reported that fastigial fibers also project to the upper cervical spinal cord, a finding which has since been overlooked. Following injection o f horseradish peroxidase (HRP) into the upper cervical spinal cord we have found numerous labeled neurons within the fastigial nucleus, indicating the existence o f a significant direct fastigiospinal pathway. To obtain further information on this pathway, we utilized retrograde axonal t ransport o f H R P to investigate the following points: (1) Is the projection f rom the fastigial nucleus to the spinal cord bilateral or unilateral? (2) Where in the fastigial nucleus are fastigiospinal cells located? (3) To what level of the spinal cord do they primarily project? Our results, described in this paper, are confirmed and extended by the physiological study which foUows 1°. Experiments were performed on 8 cats anesthetized with Nembuta l (40 mg/kg, i.p.). In 4 cats 1-6 injections of 0.2-1.0 #1 of a 50 ~ solution of H R P (Sigma, Type VI) were made into the grey matter on one side of the C8 segment using a microsyringe fitted with a glass micropipette having a tip diameter of 20-100 #m. In 2 cats similar injections were made into the grey matter at the L5 and L7 segments. In 2 other cats 0.2 /~1 injections were made into the grey and white matter on one side o f the C~ and C5 segments with a horizontal and vertical spacing of 0.3 mm to facilitate uptake of H R P by damaged axons 4. Such injections gave rise to labeling o f cells th roughout the red

Properties of a new vestibulospinal projection, the caudal vestibulospinal tract

SummaryNeurons in the caudal portions of the medial and descending vestibular nuclei and in vestibular cell group f that project to the cervical or lumbar spinal cord were located by antidromic spinal stimulation. These caudal Vestibulospinal tract (CVST) neurons have a median conduction velocity of 12 m/sec, which is well below the conduction velocities of typical lateral or medial Vestibulospinal tract (LVST, MVST) axons. The descending fiber trajectories of CVST neurons, determined by comparing thresholds for activation of each neuron from six points in the spinal white matter, were remarkably diverse. Unlike LVST and MVST axons, which are located in the ipsilateral ventral funiculi, CVST axons can be found in both the ventral and dorsolateral funiculi on both sides of the spinal cord. The CVST system is thus both anatomically and physiologically different from the LVST and MVST.