Early ontogeny of locomotor behaviour: a comparison between altricial and precocial animals
Introduction
How can some mammals and birds locomote spontaneously soon after birth or hatching while other animals require weeks to months to do so? While this question can be addressed on a variety of levels, the focus of this review is to examine the physiological and behavioural differences in early ontogeny of locomotion between precocial and altricial species.
Chicks, rats and cats are the precocial and altricial species in which early locomotor ontogeny has been best studied. While there are important differences between avian and mammalian nervous systems, the basic circuitry for locomotion has been preserved throughout vertebrate evolution such that meaningful comparisons can be made between these species. Significantly, both chicks and rats undergo a 21-day embryonic period, thus eliminating any differences with respect to the time available for prehatching/prenatal development. The most marked differences arise at hatching/birth. Most chicks are able to stand and locomote within 6–8 h after hatching, and are able to walk and run well within 24 h of hatching. Closer examination reveals that their locomotor pattern is not completely mature at this stage, however, and requires up to 7 days to mature to the adult form [52]. In contrast, the locomotor development of rats occurs over the first 2–3 weeks after birth 2, 76. Rat pups are able to crawl on postnatal day (P) 4 but cannot stand with their abdomens free off the floor until P8. Walking with full weight-supported steps occurs at P12–13 but the hindlimbs are rotated outwards during the support phase [73]. Coordinated adult-like locomotion without exorotation does not appear until P15–16. This review will investigate the possible underlying mechanisms for the differences in these developmental patterns.
The basis for producing effective locomotion in all limbed terrestrial vertebrates has been divided into three behavioural “components” [33]. In order to move overground, an animal must be able to: (1) perform locomotor movements of limbs, e.g., alternating flexion and extension of contralateral legs, (2) adapt these movements to different conditions, e.g., to accommodate uneven terrain or voluntary changes in direction, and (3) maintain equilibrium while performing locomotor movements. The anatomical and physiological requirements for each of these components during early locomotor development will be discussed in turn, introducing differences and similarities between precocial and altricial species as appropriate.
Section snippets
Animals must be able to perform locomotor movements of the limbs
It is well established in experimental animals that spinal circuitry, in the absence of supraspinal input, has the capacity to produce alternating rhythmic activity in spinal motor nerves [33]. With intact connections between spinal motoneurons and limb muscles, this activity elicits stepping behaviour in the limbs, such that a completely spinalized cat can support its weight and step on a moving treadmill [4]. Of course, in the intact animal, spinal circuits normally receive two important
Animals must be able to adapt locomotor movements for different conditions
In addition to producing basic locomotor movements with the limbs, animals must be able to make adjustments to the basic locomotor pattern in order to move overground effectively. Adjustments are necessary to adapt to uneven terrain, avoid obstacles and/or to alter the direction of movement. These changes require supraspinal control over spinal locomotor circuitry 21, 40, 79 (for reviews, see 3, 34, 62). It possible that the relatively late appearance of locomotor behaviour in altricial animals
Animals must be able to maintain posture and equilibrium during locomotion
In order to produce effective locomotion, animals must maintain equilibrium while performing locomotor movements. Equilibrium, which for these purposes is the maintenance of an upright position of the body, is accomplished using the postural muscles of the trunk and limbs. Thus, in addition to the development of vestibular system and vestibulospinal projections, the development of postural control is an essential aspect of locomotor maturation. Much information is available on the development
Conclusions
Many precocial and altricial animals are born or hatch with the ability to produce alternating stepping movements with limbs. This indicates that the basic elements underlying locomotion: (1) spinal circuitry capable of generating rhythmic alternating output, (2) sufficient supraspinal control to initiate movements, and (3) effective output to motoneurons and muscle, are therefore present prior to expression of mature overground gait in both groups of animals. Nevertheless, the notable
Acknowledgements
The author would like to thank the anonymous reviewers, whose constructive comments have led to improvements in this manuscript.
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