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  Coordinations of locomotor and respiratory rhythms in vitro are critically dependent on hindlimb sensory inputs
J Morin, D Viala
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mise à jour du
11 septembre 2003
Exp Brain Res
Convergence of central respiratory and locomotor rhythms onto single neurons of the lateral reticular nucleus
Ezure K, Tanaka I
Department of Neurobiology, Tokyo Metropolitan Institure for Neuroscience,
Fuchu, Tokyo , Japan
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Abstract We have analyzed the behavior of neurons of the lateral reticular nucleus (LRN) during fictive respiration and locomotion and found that some LRN neurons have both central respiratory and locomotor rhythms.
Experiments were conducted on decerebrate, decerebellate, immobilized, and artificially ventilated cats, with the spinal cord transected at the lower thoracic cord. Fictive respiration and fictive forelimb locomotion were ascertained by monitoring activities from the phrenic nerve and forelimb extensor and flexor nerves, respectively.
Fictive locomotion was evoked by electrical stimulation of the mesencephalic locomotor region (MLR) or sometimes occurred spontaneously. During fictive locomotion many LRN neurons fired in certain phases of the locomotion cycle; i.e., with respect to the nerve discharge of the ipsilateral forelimb they fired in either the extensor, flexor, extensor-flexor, or flexor-extensor phase.
Firing of some LRN neurons was modulated synchronously with central respiratory rhythm. Neurons with inspiratory activity and those with expiratory activity were both found. More than half of these respiration-related LRN neurons had locomotor rhythm as well.
The majority of the three types of LRN neurons, i.e., neurons with only locomotor rhythm, those with only respiratory rhythm, and those with both respiratory and locomotor rhythms, were antidromically activated by electrical stimulation of the ipsilateral inferior cerebellar peduncle. Electrical stimulation of the upper cervical cord showed that these LRN neurons, not only locomotion-related but also respiration-related neurons, received short latency inputs from the spinal cord.
The LRN neurons studied were distributed widely in the LRN, relatively densely in the caudal two-thirds of the nucleus. No particular differences were detected between the three types of LRN neurons with respect to their location in the nucleus. These results indicate that the information about central respiratory and locomotor rhythms that is necessary for cerebellar control of the coordination between respiration and locomotion converges, at least partly, at the level of the LRN.


Introduction : The lateral reticular nucleus (LRN). a major source of mossy fibers to the cerebellum, reccives inputs from a large nurnber of supraspinal motor centers and intervenes in the spino-reticulo-cerehellar pathway (SRCP), which conveys information concerning the activity of spinal motor centers. It is a large nucleus lying in the ventrolateral part of the lower medulla and adjacent to the ventral respiratory group (VRG), which plays a major role in respiraton control.
During the course of our stddy on respiratory neurons of the VRG we often recorded, largely by chance, from LRN neurons: their situation in the LRN was noticed after the experiments by histological examination. These LRN neurons often showed respiratory or locomotor rhythm and sometimes the two rhythms. Since there are few reports on their firing properties during respiratory and locomotor movements, we aimed to study the behavior of LRN neurons in more detail during these movements. In particular, there are no published reports that observed single LRN neurons, having both respiratory and locomotor rhythms.
At present, several key nuclei that participate in respiratory control have been identified in the medulla: e.g., the dorsal respiratory groups (DRG), the VRG, and the Botzinger complex. Before identification of these nuclei, early studies surveyed the medulla and pons searching for neurons that fired in synchrony with the respiratory rhythm. Some of such studies have found neurons with respiratory activity in the LRN. However, not much attention has been paid to these findings, presumably bccause the role of the cerebellum in respiration is vague and the respiration-related LRN neurons, if any, are almost certainly not involved in respiratory rhythm generation. In consequence, at present, the firing properties and distribution of the respiration-related LRN neurons are not well known.

On the other hand, more studies have been done on LRN neurons in relation to limb movements. In particular, the behavior of LRN neurons during scratching movements in the hindlimb has been studied extensively. The LRN neurons showed distinct modulation of their discharge during scratching, most of them firing in the extensor (Ex) phase of the scratching cycle. Although the LRN neUrons are known to fire in synchrony with forelimb locomotion as well. the information about their behavior during locomotion is limited compared with that during scratching.

This study concerned with the LRN neurons with respiratory and/or locomotor rhythms, describes: ( 1 ) their firing, patterns during respiration and locomotion. (2) their distribution, (3) their projections to the cerebellar peduncle and (4) inputs from the spinal cord. [...]


This study has extended the previous investigations of the activition of LRN neurons during fictive respiration and during fictive locomotion. We examined the firing properties of LRN neurons during respiration and locomotion in more detail and in addition we studied the firing of LRN neurons when respiration and locomotion occurred simultanously. In particular, this is the first report finding single LRN neurons that have both respiratory and locomotor rhythms. These findings will provide a new insight into the function of LRN neurons and the cerebellar control of respiration and locomotion.

Distribution and sampling, of the LRN neurons

The LRN is divided into three parts: a small-celled parvocellular, a large-celled magnocellular and a rostral subtrigeminal part. The parvocellular and magnocellular parts occupy the ventrolateral and dorsolateral regions of the nucleus, respectively and comprise the major portion of the LRN. The rostral and lateral part of the major portion gradually becomes the subtrigeminal part which is located immediately ventral to the spinal trigeminal tract. The rostral and medial border of the major portion of the LRN is unclear, with a gradual decrease in cell density. Moreover. the border between the parvo- and magnocellular parts can only be vaguely delimited.

The present Study intended to sample LRN neurons as widely as possible from the major portion of the LRN. The present LRN neurons were located in both the parvocellular and magnocellular parts: the neurons found in the close vicinity of the ventrolateral border of the medulla belong to the parvocellular part. However, no neurons were sampled from the lateral part of the nucleus. This could be due to sampling bias, because (1) the sampling from the lateral edge of the brainstem is technically difficult and (2) the lateral part corresponds largely to the parvocellular part consisting of small neurons. It is also possible that the lateral part of the LRN receives afferents from the spinal cord below L3 and such inputs were removed in the present study.

With the reservation mentioned above, the LRN neurons sampled were distributed throughout the rostrocaudal extent of the major portion. This is consistent with the previous results: LRN neurons modulated with forelinib locomotion were recorded throughout the LRN. In addition, the present study shows that LRN neurons related to forelimb locomotion are distributed more densely in the caudal region of the major portion of the nucleus, largely caudal to the obex. This is in contrast to the distribution of LRN neurons that respond to fictive scratching in the hindlimb: such LRN neurons are located preferentially in the rostral area of the LRN, rostral to the obex. Therefore. it is possible that the LRN neurons related to hindlimb movements are located more rostrally and those related to forelimb movements more caudally.

One hundred and five of the 122 LRN neurons tested were antidromically activated from the inferior cerebellar peduncle. Antidromic activation of some other LRN neurons was uncertain because of the follo\wing when spontaneous locomotion was present we sampled locomotion-related neurons first and then the cerebellar peduncle was stimulated to examine their antidromic responses. However, the stimulation of the cerebellar peduncle almost always evoked synchronous discharges of a large number of LRN neurons. Since LRN neurons in general had spike activity of large amplitude easily exceeding 1 mV the spikes of the isolated neuron were often obscured. In such cases, it was difficult to confirm antidromic activation even with a collision test. Nevertheless, the present results suggest that almost all the LRN neurons with respiratory and/or locomotor rhythms project to thee cerebellum considering, that the stimulating electrode could activate not all axons that passed the cerebellar peduncle. On thee other hand, when spontaneous locomotion was absent, we first idenfied LRN neurons by stimulating the cerebellar pedoncle and then locomotion was evoked by MLR stimulalion. This often activated previously quiet neurons and the spikes of the isolated neurons were contaminated by large spikes of newly recruited neurons. Then. the initially isolated neurons could not be characterized during locomotion and had to be discarded. With these experiences we tended to discard, from the begining neurons with small spikes: thus the present sampling was biased toward recording from neurons with larger spikes.

Behavior of LRN neurons during locomotion

Arshavsky and colleagues ( 1986a) have made extensive study of neurons in the spinal cord and brainstem that are related to limb movements. In particular, they have analyzed the neural mechanisms of fictive scratching that involves only one hindlimb. They have clarified many features of the input-output organization of the cerebellum as weil as the organization of thee spinal motor centers during scratching and locomotion. They studied LRN neurons because the LRN is the relay nucleus of the SRCR one of the major afferent systems ofthe cerebellum. LRN neurons show distinct modulation of their discharge in synchrony with scratching and loconiotion rhythms similarly to neurons oft he other spinocerebellar tracts.

During hindlimb scratching, most LRN neurons fire in the vicinity of the Ex phase of the scratching cycle. This firing of LRN neurons contrasts with that of ventral spinocerebellar tract (VSCT) neurons. whicli fire largely in the FI phase. Thus. it is stugested thal the two pathways to the cerchellm, the SRCP and the VSCT, convey messages about procceses occurring in different phases of the scratching cycle. Although the behavior of LRN neurons during forcelimb locomotion has been studied by using preparations similar to the present study, it has not been reported in which phase of the locomotion cycle LRN neurons fire. The present results show that there are many LRN neurons that fire in the FI phase as well in the FI-Ex and Ex-FI phases, although LRN neurons .. in fre in the Ex phase are the most abundant. A direct comparison between the present results in forlimb locomotion and the previous results in hindlimb scratching is difficult, because: ( 1 ) scratching involves only one limb and the cycle consists of short EX phase and long FI phase in contrast to the locomotion cycle; and (2) the locomotion was sudied in the forelimb and hindlimb movements. It is possiblethat the LRN neurons linked to hindlimb movements did not respond to forelimb locomotion and thus have not been studied in the present study.

The present as well as previous results obtained in immobilized animals show that the rhythmic activity of LRN neurons is of central but not peripheral origin. During hindlimn scratching this central drive originates in the motor center of the lumber cord and influences of supraspinal motor centers on LRN neurons are of minor importance. In the case of forelimb locomotion, at least one source of rhythmic input from the spinal cord has been identified Arshavsky showed thal virtually all (26 of 27) of the C3-4 propriospinal neurons (C3-4 PNs) that project to the LRN had locomotor rythm. The central drive to C3+4 PNs originatesin the cervical cord, and influences of supra spinal motors centers are of minor importance. However, it has not been reported in which phase of the locomotion cycle the C3+C4 PNs fire. Other neurons or tracts that convey information about forelimb locomotion to the LRN are not known and remain to be studied.

Behavior of LRN neurons during respiration

Gesell et al. (1936) were the first to record from single respiratory neurons in the brain making extensive tracking by fine needle electrodes. They recorded from respiratory neurons in the areas around the solitary tract and the nucleus ambiguus in the dog which at present are known as the DRG and the VRG, respectively. In this pioneering study, they recorded from both inspiratoy and expiratory neurons in the ventrolateral medulla and localized these neurons in the LRN. Vibert et al. ( 1976). who mapped respiratory neurons in the pons and medulla in the cat, also reported the existence of respiratory neurons in the LRN, although they did not describe the type of respiratory neurons recorded from.

The respiralory neurons recorded in the present study are presumably from the same population of respiratory neurons reported in the previous studies. We have added more information about their firing patterns and locations in the LRN. The respiratory rhythm in these LRN neurons is of central origin, as is the locomotor rhythm. The respiration related LRN neurons fired in the absence of rhythmical sensory inputs, which was shown by stopping the ventilator in the immobilized animal. This characteristic is similar to that of respiratory neurons of the medullary respiratory center such as the DRG VRG. and Botzinger complex. It remains to be elucidated whether the respiratory inputs are conveyed to the LRN directly from the medullary respiratory center, or indirectly via the spinal cord, or from both. There are suggesyions that some DRG neurons and swallowing-related respiratory neurons in the medulla have axon collaterars in the LRN. Antidromic mapping by electrical stimulation of decrementing inspiratory neurons and decrementing expiratory neurons of the Botzinger complexalso suggests their projections to the LRN in a few cases.

Inputs from the spinal cord

The LRN receives information from a number of ascending tracts from the spinal cord as well as from supraspinal motor centers; We stimulated the ventral part of the C3/4 spinal cord to examine whetheir or not the LRN neurons with respiratory and/or locomotor rhythms received inputs from the spinal cord. The stimulation could activate three well-studied tracts that ascend the lateralfuniculus: there are the bilateral ventral flexor reflex tract (bVFRT), the ipsilateral fore-limb tract (iFT) and ascending branches or somata of the C3-4 PNs. The short-latency responses in more than 70% of LRN neurons from the ipsilateral C3/4 cord are consistent with the resuslts that the LRN neurons receive monosynaptic inputs from these tracts.

The latencies shorter than 2 ms in fig 10 suggest monosynaptic activation from the bVFRT and iFT. Since the conduction velocities of the ascending branches of the C3-4 PNs are about twice as slow as those of the bVFRT and iFT, the latencies shorter than 4 ms in Fig. 10 may also be within the monosynaptic range.

A large portion of the monosynaptic connections from both the bVFRT and the iFT to LRN neurons are inhibitory. Although the present extracellular study hardly detected such inhibitory connections, it is highly probable that many of the present LRN neurons had monosynaptic inhibitory inputs from the spinal cord. The above argument holds only for the ipsilateral stimulation. It is difficult to compare the present contralateral stimulation with that of the previously studies.

In the previously studies, in all cases. the spinal cord contralateral to the LRN was transected at C2-3. The contralateral stimulation in such preparations activated descending pathway,. in particular the vestibulospinal tract which excites monosynaptically the bVFRT neurons terminating in the contralateral LRN. In contrast, the present experimental situation was too complicated, activating both descending and ascending tracts. Nevertheless, the short-latency responses from the contralateral spinal cord suggest the existence of monosynaptic ascending connections, which have not been specified yet.

Respiration. locomotion, and cerebellum

The cerebellum receives at least two sorts of information from the spinal cord during limb movements. One is the information from peripheral sensory apparatus and it is used to monitor on-going movements. The other is the information about the activity of spinal motor centers. During hindlimb movements, the former is carried by the dorsal spinocerebellar tract (DSCT) and the latter by the VSCT. During forelimb movements, respective information is carried by the cuneocerebellar tract (CCT) and the rostral spinocerebellar tract (RSCT). In addition to these direct spinocerebellar tracts, the indirect spinocerebellar pathway through the LRN, i.e.. the SRCP exists. The SRCP carries information about the activity of spinal motor centers rather than the activity of peripheral sensory apparatus.

In this respect, the respiratory system is organizedsimilarly to the locomotor or scratching system. Hirai and colleagues found two spinocerebellar tracts that convey rhythmic respiratory information. Some DSCT neurons located in Clark's column were shown to have respiratory rhythm and ascend ipsilaterally. These DSCT neurons receive peripheral inputs that respond to movernents of the chest wall. A group of neurons located in laminae VII and VIII of the thoracic spinal cord were found to have respiratory rhythm and to ascend in the contralateral spirial cord. In contrast with the DSCT neurons, the firing of these neurons is modulated by central respiratory driv, some of them receiving additional peripheral inputs. As shown in the present study, the path through the LRN also carries respiratory information to the cerebellum. In addition to these inputs, the pathway through the inferior olivary nucleus functions in the respiratory system as well as in the limb movement system.

Respiration-related neurons are recorded from both cerebellar cortex and nuclei. Involvement of the cerebellum in control of respiration is evident from stimulation and lesion studies. However. the role of the cerebellum in respiration has not been established. It is suggested that the cerebellum functions not only in postural reflexes but also in respiratory, cardiovascular, and other autonomic reflexes. In particular, respiratory and locomotor inputs to the cerebellum may function in homeostatic adjustments of respiratory movements during locomotion, and this may he revealed as interactions between central rhythm generators of respiration and locomotion.

The present study has shown that respiratory and locomotor inputs to the cerebellum converge, at least partly. on the LRN neurons. Furthermore, LRN neurons are known to have conjoint inputs, from macular and neck receptors, and may function in control of neck, limbs and extrinsic eye musculature. Since a large nimber (more then 50%) of the LRN neurons studied have convergent neck and macular inputs, it is quite possible that other inputs, e.g., respiratory and locomotor inputs, also converge on these LRN neurons. If this is this case, single LRN neurons relay a large number of inputs of various modalities to the cerebellum.

Comprendre avec l'aide de K Ezure la coordination respiration - marche
Convergence of central respiratory and locomotor rhythms onto single neurons of the lateral reticular nucleus Ezure K, Tanaka I Exp Brain Res1997; 113; 2; 230-242
Respiratory and locomotor patterns