Flexibility of the axial central pattern generator network for locomotion in the salamander

Abstract

In tetrapods, limb and axial movements are coordinated during locomotion. It is well established that inter- and intralimb coordination show considerable variations during ongoing locomotion. Much less is known about the flexibility of the axial musculoskeletal system during locomotion and the neural mechanisms involved. Here we examined this issue in the salamander Pleurodeles waltlii, which is capable of locomotion in both aquatic and terrestrial environments. Kinematics of the trunk and electromyograms from the mid-trunk epaxial myotomes were recorded during four locomotor behaviors in freely moving animals. A similar approach was used during rhythmic struggling movements since this would give some insight into the flexibility of the axial motor system. Our results show that each of the forms of locomotion and the struggling behavior is characterized by a distinct combination of mid-trunk motor patterns and cycle durations. Using in vitro electrophysiological recordings in isolated spinal cords, we observed that the spinal networks activated with bath-applied N-methyl-d-aspartate could generate these axial motor patterns. In these isolated spinal cord preparations, the limb motor nerve activities were coordinated with each mid-trunk motor pattern. Furthermore, isolated mid-trunk spinal cords and hemicords could generate the mid-trunk motor patterns. This indicates that each side of the cord comprises a network able to generate coordinated axial motor activity. The roles of descending and sensory inputs in the behavior-related changes in axial motor coordination are discussed.

The mesencephalic locomotor region sends a bilateral glutamatergic drive to hindbrain reticulospinal neurons in a tetrapod

“…They also receive an indirect MLR input through the activation of a group of brainstem muscarinoceptive cells that in turn send an additional excitation to RS cells (Smetana et al, ). In salamanders, the spinal locomotor networks can also be activated by pharmacologically mimicking the descending RS drive with glutamatergic agonists (Wheatley et al, ; Cheng et al, ; Delvolvé et al, ; Ryczko et al, ; Charrier and Cabelguen, ). The anatomy of the RS system was described in this animal by tracing studies (Naujoks‐Manteuffel and Manteuffel, ; Sanchez‐Camacho et al, ; Hubbard et al, ) and some RS cells were shown to be glutamatergic (Chevallier et al, ).…”

Interfacing a salamander brain with a salamander-like robot: Control of speed and direction with calcium signals from brainstem reticulospinal neurons

“…To this end we used the salamander as an animal model, where the brainstem networks are easily accessible experimentally. In salamanders as in other vertebrates, the basic muscle contractions are programmed by a specialized neural network in the spinal cord called the Central Pattern Generator (CPG, see [25]), which controls axial and limb movements [26], [27], [28], [29]. This network integrates sensory signal and is under the control of brainstem locomotor networks.…”

Towards an Understanding of Control of Complex Rhythmical ‘Wavelike’ Coordination in Humans

“…In both butterfly swimming and front crawl swimming the sequencing of joint rotations leads to wavelike transmission of motion caudally as indicated by, and determined by, the phase differences between adjacent body parts [12,15]. While it is useful to compare control of these wavelike motions to that of other species it is also necessary to recognize that control of cephalo-caudal wave propagation by CPGs to produce undulating waves along the spine of animals such as Lamprey [31], and salamander [38] amphibians, quadraped mammals, and primates. Indeed this review has revealed organizational models with commonalities among species including Lamprey [31], salamander [38] and crayfish [39][40], and in mammals such as rats [33,42], mice [43] and cats [30,34].…”

“…Given these results, it is intriguing that in both front crawl and butterfly swimming, complex phase relationships that are essential to optimize performance are maintained across cycles and that these phase relationships are maintained for body and segmental rotations of different oscillation frequencies.Axial progression of body waves has been shown in limbless marine animals and in-vitro spines of tetrapods. For example, Ryczko et al[38] used video-based kinematic analysis and indwelling EMG of the axial musculature to establish that body waves progress along the bodies of freely moving salamanders and that the nature of the waves varies according to the task. When swimming, or backward stepping, waves travelled posteriorly and corresponded to propagation of waves of EMG that travelled at a faster rate than the kinematic wave.…”