Splenius Motoneurons Research Articles

Nonuniform distribution of contacts from noradrenergic and serotonergic boutons on the dendrites of cat splenius motoneurons

The input-output properties of motoneurons are dynamically regulated. This regulation depends, in part, on the relative location of excitatory and inhibitory synapses, voltage-dependent and -independent channels, and neuromodulatory synapses on the dendritic tree. The goal of the present study was to quantify the number and distribution of synapses from two powerful neuromodulatory systems that originate from noradrenergic (NA) and serotonergic (5-HT) neurons. Here we show that the dendritic trees of motoneurons innervating a dorsal neck extensor muscle, splenius, in the adult cat are densely, but not uniformly innervated by both NA and 5-HT boutons. Identified splenius motoneurons were intracellularly stained with Neurobiotin. Using 3D reconstruction techniques we mapped the distributions of contacts formed by NA and 5-HT boutons on the reconstructed dendritic trees of these motoneurons. Splenius motoneurons received an average of 1,230 NA contacts (range = 647-1,507) and 1,582 5-HT contacts (range = 1,234-2,143). The densities of these contacts were 10 (NA) to 6 (5-HT)-fold higher on small compared to large-diameter dendrites. This relationship largely accounts for the bias of NA and 5-HT contacts on distal dendrites and is partially responsible for the higher density of NA contacts on dendrites located more than 200 μm dorsal to the soma. These results suggest that the neuromodulatory actions of NA and 5-HT are compartmentalized and regulate the input-output properties of motoneurons according to precisely arranged interactions with voltage-dependent and -independent channels that are primarily located on small-diameter dendrites.

Distribution of vestibulospinal contacts on the dendrites of ipsilateral splenius motoneurons: An anatomical substrate for push-pull interactions during vestibulocollic reflexes

Excitatory and inhibitory synapses may control neuronal output through a push-pull mechanism—that is, increases in excitation are coupled to simultaneous decreases in inhibition or vice versa. This pattern of activity is characteristic of excitatory and inhibitory vestibulospinal axons that mediate vestibulocollic reflexes. Previously, we showed that medial vestibulospinal tract (MVST) neurons in the rostral descending vestibular nucleus (DVN), an excitatory pathway, primarily innervate the medial dendrites of contralateral splenius motoneurons. In the present study, we tested the hypothesis that the counterparts of the push-pull mechanism, the ipsilateral inhibitory MVST synapses, are distributed on the dendritic tree such that the interactions with excitatory MVST synapses are enhanced. We combined anterograde tracing and intracellular staining in adult felines and show that most contacts (∼ 70%) between inhibitory MVST neurons in the rostral DVN and ipsilateral splenius motoneurons are also located on medial dendrites. There was a weak bias towards proximal dendrites. Using computational methods, we further show that the organization of excitatory and inhibitory MVST synapses on splenius motoneurons increases their likelihood for interaction. We found that if either excitatory or inhibitory MVST synapses were uniformly distributed throughout the dendritic tree, the proportion of inhibitory contacts in close proximity to excitatory contacts decreased. Thus, the compartmentalized distribution of excitatory and inhibitory MVST synapses on splenius motoneurons may be specifically designed to enhance their interactions during vestibulocollic reflexes. This suggests that the push-pull modulation of motoneuron output is based, in part, on the spatial arrangement of synapses on the dendritic tree.

Effect of localized innervation of the dendritic trees of feline motoneurons on the amplification of synaptic input: a computational study

Previous studies show that the activation of voltage-dependent channels is dependent on the local density of synapses in the dendritic region containing voltage-dependent channels. We hypothesized that the selective innervation of excitatory vestibulospinal (VST) neurons on the medial dendrites of contralateral splenius motoneurons is designed to enhance the activation of persistent inward currents (PICs) mediated by dendritic L-type Ca(2+) channels. Using compartmental models of splenius motoneurons we compared the synaptic current reaching the soma in response to excitatory input generated by synapses with two different distribution patterns. The medial distribution was based on the arrangement of VST synapses on the dendrites of contralateral splenius motoneurons and the uniform distribution was based on an arrangement of synapses with no particular bias to any region of the dendritic tree. The number of synapses in each distribution was designed to match estimates of the number of VST synapses activated by head movements. In the absence of PICs, the current delivered by the synapses in the uniform distribution was slightly greater. However, the maximal currents were small, < or = 4.1 nA, regardless of the distribution of synapses. In models equipped with L-type Ca(2+) channels, PIC activation was largely determined by the local density of synapses in proximity to the L-type Ca(2+) channels. In 3 of 5 cells, this led to a 2- to 4-fold increase in the current generated by synapses in the medial distribution compared to the uniform distribution. In the other two cells, the amplification bias was in favour of the medial distribution but was either small or restricted to a narrow range of frequencies. These simulations suggest that the innervation pattern of VST axons on contralateral splenius motoneurons is arranged to strengthen an otherwise weak synaptic input by increasing the likelihood of activating PICs. Additional simulations suggest that this prediction can be tested using common experimental protocols.

Direct connection of the nucleus reticularis gigantocellularis neurons with neck motoneurons in cats.

Functional connections of single reticulospinal neurons (RSNs) in the nucleus reticularis gigantocellularis (NRG) with ipsilateral dorsal neck motoneurons were examined with the spike-triggered averaging technique. Extracellular spikes of single NRG-RSNs activated antidromically from the C6, but not from the L1 segment (C-RSNs) were used as the trigger. These neurons were monosynaptically activated from the superior colliculus and the cerebral peduncle. Single-RSN PSPs were recorded in 43 dorsal neck motoneurons [biventer cervicis and complexus (BCC) and splenius (SPL)] for 21 NRG-RSNs and 135 motoneurons tested. All synaptic potentials were EPSPs, and most of their latencies, measured from the triggering spikes, were 0.8-1.5 ms, which is in a monosynaptic range. The amplitudes of single-RSN EPSPs were 10-360 microV. Spike-triggered averaging revealed single-RSN EPSPs in multiple motoneurons of the same species (SPL or BCC), their locations extending up to nearly 1 mm rostrocaudally. Synaptic connections of single RSNs with both SPL and BCC motoneurons were also found with some predominance for one of them. The results provide direct evidence that NRG-RSNs make monosynaptic excitatory connections with SPL and BCC motoneurons. It appears that some NRG-RSNs connect predominantly with SPL motoneurons and others with BCC motoneurons.

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)

Pyramidal effects in dorsal neck motoneurones of the cat.

The effects of contralateral pyramidal stimulation have been investigated with intracellular recording from cat alpha-motoneurones that innervate the dorsal neck musculature. A short train of stimuli evoked three types of synaptic effects: predominant excitation or inhibition and mixed effects characterized chiefly by early excitation followed by inhibition. Latency measurements indicated a minimal disynaptic linkage for excitation and for inhibition. Splenius motoneurones received primarily excitation whereas biventer cervicis-complexus motoneurones received a more varied input characterized by mixed effects or inhibition. Following transection of the pyramid just rostral to the decussation (lower pyramidal lesion) pyramidal stimulation above the lesion still produced disynaptic excitation and longer latency (possibly trisynaptic) inhibition. Pyramidal stimulation just caudal to this transection evoked inhibition with a minimal disynaptic latency, as well as longer latency excitation. The incidence of longer latency excitation was found to be reduced in cats with corticospinal tract transections at the level of the second cervical spinal segment. No post-synaptic potentials were evoked by pyramidal stimulation rostral to a pyramidal transection at the level of the trapezoid body. It is suggested that disynaptic excitation evoked by pyramidal stimulation above the lower pyramidal lesion is mediated by medullary reticulospinal neurones possessing monosynaptic excitatory connexions with neck motoneurones. Longer latency excitation appears to be mediated by neurones that receive corticospinal tract input and are located in the spinal segments containing the neck motoneurones. Disynaptic inhibition is mediated by neurones likely to be situated between the second cervical spinal segment and the level of the lower pyramidal lesion. The results also suggest that the first neurone in the chain mediating longer latency inhibition is located in the brain stem. The differences in pyramidal synaptic input between splenius and biventer cervicis-complexus motoneurones are considered in relation to the roles these muscles may serve in head position control.

Dendritic distribution of splenius motoneurons in the cat: comparison of motoneurons innervating different regions of the muscle.

The distribution and dendritic organization of splenius motoneurons innervating extrafusal muscle fibers in different regions of the muscle were examined by electrophysiological and intracellular HRP staining techniques. Motoneurons innervating the regions of the splenius muscle supplied by the C2, C3, and C4 peripheral nerves were arranged in three nonoverlapping subnuclei. Reconstructions of the dendritic trees of splenius motoneurons in these three subnuclei showed that there were no major differences in their dendritic distributions. Instead, the dendritic distribution followed a single pattern which was composed of five major dendritic projections. These included a dorsolateral projection to the lateral part of lamina VIII, a lateral projection into the spinal accessory nucleus and beyond the gray-white border, ventral and ventrolateral dendrites in the lateral half of the ventromedial nucleus and the surrounding white matter, medial dendrites which projected both dorsally and ventrally, and finally a conspicuous collection of dendrites which projected rostrally and caudally from the cell body. These results indicate that the dendritic distributions of splenius motoneurons are not related to the segmental position of the motoneuron or the zone of the muscle innervated by the motoneuron. However, a comparison of the dendritic distribution of splenius motoneurons to the dendritic distribution of biventer cervicis-complexus motoneurons indicated that there are major differences in the form of their dendritic trees even though dendrites from both sets of motoneurons share the same territory. As a consequence, although these motoneurons may receive the same connections, the effect of these connections on the excitability of the motoneurons may differ.

Reflex connexions of motoneurones of muscles involved in head movement in the cat.

1. The reflex connexions from muscle afferents and ventral root fibres to the motoneurones of the muscles biventer-cervicis, complexus, sternocleidomastoid, trapezius and splenius, the principal muscles involved in head movement in the cat, were studied with the technique of intracellular recording. 2. Electrical stimulation of homonymous muscle afferents of biventer-cervicis and complexus, sternocleidomastoid and trapezius, at strengths below 1.6 times threshold of the dorsal root afferent volley, produced monosynaptic e.p.s.p.s in the corresponding motoneurones. Recruitment of higher threshold muscle afferents produced additional p.s.p.s with longer central delays. 3. Stimulation of low-threshold muscle afferents did not produce any p.s.p.s in the motoneurones of the ipsilateral antagonist. Stimulation of higher threshold afferents evoked i.p.s.p.s with central delays longer than 1.6 msec, or mixed e.p.s.p.-i.p.s.p.s in the ipsilateral antagonist. 4. Mixed e.p.s.p.-i.p.s.p.s or i.p.s.p.s with central delays longer than 1.5 msec were evoked in trapezius motoneurones upon stimulation of high threshold afferents from biventer-cervicis and complexus, while stimulation of low-threshold biventercervicis and complexus afferents evoked no p.s.p.s in trapezius motoneurones. 5. Stimulation of contralateral low-threshold biventer-cervicis and complexus afferents evoked a sequence of i.p.s.p. disinhibition in sternocleidomastoid motoneurones, and vice versa, with central delays longer than 1.7 msec. 6. Stimulation of the deafferented biventer-cervicis, complexus, splenius, sternocleidomastoid and trapezius muscle nerves frequently activated interneurones in the ventral horn at monosynaptic central delays. Activation of homoynmous ventral root fibres rarely evoked p.s.p.s in biventer-cervicis, complexius, splenius or sternocleidomastoid motoneurones, while it produced disynaptic i.p.s.p.s in 80% of trapezius motoneurones. 7. It is concluded that Ia reciprocal inhibition and recurrent inhibition, two reflex circuits which are so prominent in limb segments of the spinal cord, do not play a major role in the generation of head movement. Rather, head movement may be primarily controlled from supraspinal centres.

Semicircular Canal and Macular Influences on Neck Motoneurons

Publisher Summary This chapter highlights the influences of semicircular canal and macular on neck motoneurons. Synaptic potentials were recorded in cat dorsal neck motoneurons in response to stimulation of individual ampullary nerves or macular nerves. Disynaptic excitatory postsynaptic potential (EPSP) and inhibitory postsynaptic potential (IPSPs) were seen in dorsal neck motoneurons by stimulation of individual ampullary nerves. The early disynaptic potentials were usually followed by later components. Dorsal neck motoneurons are excited by stimulation of the two anterior canals, inhibited from the two posterior ampullae. A majority of these motoneurons were inhibited from the ipsilateral, excited from the contralateral horizontal canal. Splenius motoneurons are influenced most consistently from the horizontal canal. Stimulation of the saccular nerve usually evoked IPSPs in contralateral, EPSPs in ipsilateral neck motoneurons. Many of the potentials were probably disynaptic, though some were trisynaptic. The effects of utricular nerve were complex, perhaps because of contamination by canal afferents. The predominant effects consisted of ipsilateral inhibition and contralateral excitation.

Distribution of motoneurones to the neck muscles, biventer cervicis, splenius and complexus in the cat.

The distribution of motoneurones to the cat dorsal neck muscles biventer cervicis, splenius and complexus has been examined using the technique of retrograde horseradish peroxidase transport. A comparison was initially made of HRP uptake into motoneurones produced either by injecting HRP solution directly into a single neck muscle or by exposing the cut ends of motor nerves to an HRP solution. The injection of HRP into single neck muscles was found to produce widespread labelling of motoneurones presumably due to diffusion of HRP into adjacent muscles. For the examination of individual motoneurone pools the technique of cut nerve exposure was therefore used. Labelled neck muscle motoneurones ranged from 10-70 mu in diameter, but the majority of cells had diameters which were less than 40 mu. Most cells were located in the ventromedial nucleus and along the medial border of the ventral horn. In these regions there was considerable overlap between the motoneurone pools of the three neck muscles examined. In addition, some splenius motoneurones were located in the nucleus of the spinal accessory nerve. Labelled neck muscle motoneurones were also located in areas not usually considered to contain motoneurones such as the commissural and centrodorsal nuclei and in the ventral commissure.

Direct excitation of neck motoneurons by interstitiospinal fibers

1. 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.

Segmental reflex inputs to motoneurons innervating dorsal neck musculature in the cat.

The responses to stimulation of upper cervical muscle and cutaneous afferents were studied in motoneurons innervating splenius, complexus, and biventer cervicis dorsal neck muscles of cats. Motoneurons innervating complexus and biventer cervicis fibers, which are in the deeper, longitudinally oriented muscles, were monosynaptically excited by ipsilateral Group I afferents from each of these muscles, but they did not receive significant input from splenius Group I afferents. Likewise, splenius motoneurons were not monosynaptically excited by ipsilateral afferents from complexus anf biventer cervicis. Stimulation of ipsilateral cutaneous afferents produced predominant excitation in splenius motoneurons, predominant inhibition in biventer cervicis motoneurons, and inhibition or mixed responses in complexus motoneurons. None of the neck motoneurons studied showed postsynaptic potentials following single or multiple shock stimulation of contralateral muscle nerves at stimulus intensities expected to excite exclusively Group I afferents. Higher intensity stimulation of contralateral muscle afferents, as well as fibers in the greater auricular nerves, produced predominant inhibition in all three neck motoneuron pools. Segmentally-excited afferents to neck motoneurons, like those from supraspinal systems, appear to evoke different patterns of synaptic responses in splenius motoneurons than they do in motoneurons innervating fibers in the deeper, longitudinally oriented complexus and biventer cervicis muscles.