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The fundamental evolutionary change in Vertebrate locomotion that allowed the transformation from aquatic swimming to overground stepping was related to a substantial reshaping of locomotor rhythm generating circuits located at the spinal cord level. The metameric organization of rhythm genesis in the lamprey, for example, evolved into neuronal pattern-generators re-centred at C7–T1 and L1–L2 spinal levels that are responsible for driving limb locomotor movements in quadrupeds such as the rat and rabbit. In Mammals, further locomotor adaptations such as the hopping hindlimb coordination in the rabbit, which is morphologically related to hindlimb lengthening, is achieved by a supraspinal reconfiguration of the basic alternate coupling of the bilateral lumbar locomotor generators found in all studied Mammals, including the rabbit. In this way therefore, evolution and behavioural adaptation of locomotion may involve utilisation of different neural mechanisms. .
Locomotor patterns are diversified in Vertebrates and are necessarily adapted to an animal's environment and the way it feeds. The most drastic evolutionary alteration in locomotion has been associated with the change of habitat from aquatic to terrestrial living. This was in turn correlated with the appearance of limbs that became the main instruments of locomotion, replacing a fusiform body that propelled the aquatic animal by rostro-caudal undulatory waves. Even in limbed vertebrates, however, the locomotor pattern can be adapted to the development of morphological differences from the usual body plan. For instance, while most Mammals walk at low locomotor rates and gallop at high speed, a few species with substantially lengthened hindlimbs relative to their forelimbs (kangaroo, gerbil and rabbit) hop with bilaterally-synchronous hindlimb movements at all speeds. Locomotor adaptations of other limbed vertebrates can be considerably more varied than this example
In this brief synthesis, interest is focused on the evolution and adaptation of neural pattern generators responsible for such different forms of locomotion. It was originally thought that mammalian locomotion is patterned at the spinal level via peripheral reflex processes
Swimming in the lamprey, as in other fish, is achieved via waves of body contraction that propagate from the head to the tail (
Thus in a low aquatic vertebrate such as the lamprey, and probably also in other swimming vertebrates, the general metameric organization of locomotion is supported by a neural drive from segmentally distributed CPGs within the spinal cord.
Compared to the lamprey, mammalian evolution has mainly seen a re-centring of locomotor motions to the limb level, with more complex movement patterns now due to interplay between antagonistic flexor and extensor muscles to achieve normal stepping. With this evolutionary specialization of locomotion, how did the metameric CPGs of fish evolve to now drive localized appendicular parts of the body?
To a large extent, answers have been obtained from in vitro isolated brainstem-spinal cords of new born rats. (This perinatal model has been used because the high metabolic rate of Mammals does not allow survival of adult rat spinal cords in vitro.) Locomotor-like bursts were obtained from recordings on lumbar ventral roots (VRs) after a perfusion of a cocktail of NMDA and 5-HT that was at first limited to the L1 and L2 segments (
Our investigations at the cervico-thoracic level of the same pharmacologically-activated preparations have also confirmed the restricted localization (limited to C7–C8–T1 levels) of the CPGs for forelimb locomotion
To summarize therefore, in the newborn rat, locomotor-like rhythmogenesis is limited to a few spinal segments – L1–L2 and C7–T1 – that organize the limb locomotor pattern. Rhythmic activity at all other spinal levels essentially is passive and results from a drive from the rostral and caudal CPGs themselves.
Most Mammals, like the cat, the dog and the rat walk at relatively low speeds, moving their hindlimbs and forelimbs in alternation at each girdle. As described above, this alternating bilateral pattern is programmed centrally at the spinal level
In the adult rabbit, in vivo recordings of both hindlimb locomotor activity in decerebrate, curarized preparations reflected the hopping pattern of the intact animal: bilateral flexor bursts occur synchronously and in anti-phase with bilateral extensor bursts (
An interesting adaptation of the locomotor pattern to accommodate hindlimb lengthening occurs over a short period in the infant rabbit, from day 10 to 20 after birth. When the infant begins to leave the mother's nest at about 10 days, the fore- and hindlimbs are still roughly the same length and the young animal walks like a digitigrade cat. Within the ten following days, however, hindlimb hopping begins and is expressed more and more frequently in the young animal's walking pattern. At about 20 days after birth, the hindlimbs have grown much more rapidly than the forelimbs and the long hindfeet are now uniquely involved in a plantigrade hopping motion
This period of 10 to 20 days of life is important in the rabbit's life since, as reported by Langworthy
These results demonstrate that shortly after birth, the bilateral spinal pattern of hindlimb locomotion in the rabbit is a
From a comparison of the evolutionary changes in Vertebrate locomotion and its adaptation in Mammals, it emerges that the neural mechanisms involved in the two processes are not the same. The basic neural phenomenon for locomotion found in all studied vertebrates is that rhythm genesis is achieved within the spinal cord via CPGs. The aim here was to show that with evolution, the organization of the CPGs throughout the cord, which is relatively uniform and metameric in swimming low vertebrates, has become re-centred in walking Mammals to segments controlling the limbs, with a loss of rhythmogenic capacity of most other metamers. In the example of behavioural adaptation described in the hopping rabbit, the basic spinal organization is maintained exactly as in most other walking Mammals. In the rabbit, however, the hopping adaptation is obtained via a supraspinal control from the brainstem onto the spinal couplings that link left and right lumbar CPGs. While the bilateral pattern could be experimentally induced by behavioural conditioning of infant spinal rabbits, such an adaptation at the spinal level does not occur spontaneously. In this context it would be interesting to know whether the concept of employing different fundamental mechanisms in evolution and adaptation could be extended to other basic functions. To examine this possibility, Amphibians certainly represent a remarkable model of short-term evolutionary/adaptive processes that include drastic morphological and physiological changes that occur simultaneously to transform the same lamprey-like swimming tadpole into a walking (rat-like) or hopping (rabbit-like) adult
I am very grateful to Dr John Simmers for his valuable revision of the manuscript.
Locomotor organization in the lamprey. (
Fig. 1. Organisation locomotrice chez la lamproie. (A) Lamproie intacte (INTACT) schématisée montrant l'emplacement des enregistrements électromyographiques (partie droite des segments R5, R25, R45 et gauche L25). À côté, les barres horizontales en gras schématisent la durée de chaque activation musculaire en R5, R25 et R45 et montrent le retard d'activation rostro-caudal ainsi que l'alternance bilatérale entre R25 et L25. (
Locomotor genesis in the lumbar cord of the neonatal rat. In vitro preparation and local activation with NMDA and 5-HT at L1–L2 in
Fig. 2. Genèse locomotrice dans la moelle lombaire du rat nouveau-né. Préparation in vitro activée localement par le NMDA et le 5-HT: en L1-L2 en
Rhythmogenic capacity of the in vitro isolated cord of the new-born rat after activation with NMDA and 5-HT. Motor activity was recorded on homolateral ventral roots at cervical C8, thoracic T4, T7 or T8, and lumbar L1 or 2.
Fig. 3. Capacités rythmogènes de la moelle de rat nouveau-né isolée, en préparation in vitro, et totalement activée pharmacologiquement (NMDA et 5-HTP). Activités motrices enregistrées sur les racines ventrales homolatérales C8, T4, T7 ou 8, L1 ou 2.
Locomotor pattern of both hindlimbs in a decerebrate (
Fig. 4. Organisation locomotrice bilatérale au niveau des membres postérieurs chez le lapin en préparation décérébrée, puis spinale. Les décharges rythmiques sont enregistrées sur des nerfs musculaires (fléchisseur, Fl et extenseur, Ex) des membres postérieurs gauche (l) et droit (r). En (
Conditioning of the hindlimb bilateral locomotor pattern in infant rabbits spinalized shortly after birth.
Fig. 5. Conditionnement de l'organisation bilatérale au niveau des membres postérieurs chez le lapereau spinalisé rapidement après la naissance.