Within the brainstem of the lamprey is a group of neurons forming the mesencephalic locomotor centre1. These neurons project to the spinal cord and not only initiate and maintain locomotion by activating the locomotor network via the conditional pacemaker neurons described above, but can also stop it2.
The locomotor neurons in the brainstem trigger the oscillations in the spinal conditional pacemaker interneurons by releasing the excitatory amino acid transmitter, glutamate. Normally, the mesencephalic locomotor centre activates the more cranial spinal segments at higher frequencies, consequently driving sequentially the coupled oscillators of the spinal cord from the head to the tail. This pattern of activation ensures propagation of the contractions, resulting in forward swimming.
The mesencephalic neurons not only send descending projections to the locomotor spinal networks at every segment but they also receive ascending inputs from the same spinal circuits. These ascending and descending pathways complete entirely neural internal loops that are superimposed on the spinal neuromechanical loops.
This represents an important early step in the evolution of a more complex architecture of the nervous system, placing group of neurons, in this case the locomotor centre neurons, some synaptic steps away from the external world.
The architecture of superimposed neural loops enables locomotion to be affected not only by the movements initiated by the spinal locomotor net via the interconnected neuromechanical loops, but also by other special sensory inputs. Among these are the special sensory receptors for vision and balance. Visual inputs reach the locomotor centre in the brain stem and modulate the direction of swimming, usually away from the source of light. Vestibular inputs modify outputs from the locomotor centre to maintain orientation with respect to gravity. Thus, the nervous system of the lamprey is organised as a hierarchy of superimposed neural loops, which enable lampreys to navigate the world, crossing oceans and swimming up rivers.
Adapted from Grillner et al (1995).3
The linkages between neuromechanical loops and intrinsic neural activity marks the beginning of reciprocal interactions between neural circuits of organisms and the external world. The closing of the neuromechanical loop generates behaviour which is interactive with the environment and engenders a greater degree of autonomy of the organisms. This biological machinery represents a primordial mechanism for neural organisms to acquire increasing degrees of independence from the environment and marks the beginning of the processes of acquiring experiences. Thus, the lamprey, as in all vertebrates since, became capable of initiating motor activity and to responding to the environment in which they move, including the consequences of their own behaviour.
The same fundamental network can generate swimming or walking: the architecture involves superimposed loops.
Adapted from Bem et al (2003)4.
The physics suitable to describe the neural activity underlying the lamprey’s swimming is the one that applies to active media as discussed above. Thus, the interconnected spinal locomotor network behaves as an active medium with ongoing rhythmic activity following the rules of coupled oscillators with the direction of propagation determined by the frequency gradient of the segmental oscillators.
I propose that, not only in the lamprey, but in all vertebrates, the central nervous system is organised as a hierarchical system of neural loops superimposed on the primordial neuromechanical spinal loops.
- For the corresponding region in humans, see: https://en.wikipedia.org/wiki/Mesencephalic_locomotor_region
For an overview of the mesencephalon, see: https://en.wikipedia.org/wiki/Midbrain ↩︎ - F Brocard & R Dubuc (2003): Differential contribution of reticulospinal cells to the control of locomotion induced by the mesencephalic locomotor region. Journal of Neurophysiology 90, 1714–1727.
L Juvin et al (2016): A specific population of reticulospinal neurons controls the termination of locomotion. Cell Reports 15, 2377-2386.
S Grätsch et al (2019): A brainstem neural substrate for stopping locomotion. Journal of Neuroscience 39, 1044-1057. ↩︎ - S Grillner et al (1995): Neural networks that co-ordinate locomotion and body orientation in lamprey. Trends In Neuroscience 6, 270-279. ↩︎
- T Bem at al (2003): From Swimming to walking: a single basic network for two different behaviors. Biological Cybernetics 88, 79-90. ↩︎