The lamprey is one of the primitive types of jawless vertebrates (Cyclostomes) that appeared some 360 million years ago in the rivers and oceans and little changed since.
Painting by Ellen Edmonson https://en.wikipedia.org/wiki/Lamprey#/media/File:Petromyzon_marinus.jpg
The spinal cord of the lamprey contains 100 segments, each associated with a set of muscles on each side of the body. Swimming of the lamprey involves three important features1:
- the muscles of every segment undergo rhythmic contractions generated in the spinal cord and transmitted to the muscle by motor neurons;
- the rhythmic contractions alternate on the right and left sides of the body;
- the contractions propagate along the spinal segments from head to tail.
This neuromuscular pattern generates the swimming. The spatiotemporal organisation of the swimming of the lamprey can be appreciated clearly by plotting the spatiotemporal map of muscle contractions during the swimming.
A remarkable series of experiments by Sten Grillner and colleagues over the past decades has revealed the details of the neural mechanisms underlying the swimming behaviour of the lamprey. The swimming motor pattern is preserved even when the lamprey’s brain is removed. The fully isolated spinal cord with no muscles attached shows patterns of motor neuron activity that correspond to swimming activity. The three features of swimming (ie rhythmic activity, alternation right left and propagation head to tail) are retained and was thus named ‘fictive swimming’ or the ‘neural correlate‘ of swimming2.
Taking advantage of this unique feature of the spinal cord of the lamprey, neurophysiologists could use microelectrodes to record the electrical activity of single neurons in the spinal cord during fictive swimming and establish how they are interconnected3. Consequently, the neural wiring of these spinal locomotor circuits has become one of the best-known in vertebrates.
Some spinal interneurons show pacemaking activity, but only when exposed to chemicals that activate receptors for the excitatory amino acid neurotransmitter, glutamate. Thus, these spinal neurons behave as conditional pacemakers, and oscillate in the range of 0.1 to 10Hz which corresponds to the frequency of swimming of the lamprey. This rhythmic activity is shared by locomotor circuits in most vertebrates.
These slow oscillations of the neural membrane potential are due to the presence of two unique membrane proteins, one is the glutamate receptor, and the other is a channel for potassium that is sensitive to intracellular calcium concentration. When activated, the glutamate receptors depolarise the membrane of spinal neurons by letting in both sodium and calcium ions. The calcium that accumulates inside the cell in turns opens another protein, a channel for potassium ions which exit the cell, returning the membrane back to its negative resting potential. This results in the slow (0.1 – 10Hz) oscillations of membrane potential with bursts of fast action potentials superimposed on the crest of each oscillation. The oscillating activity drives the spinal cord circuits to generate rhythmic muscle contractions that alternate on the left and right sides due to the involvement of reciprocal inhibitory interneurons. Propagation from head to tail is controlled by descending interneurons that couple each segmental spinal locomotor circuit.
The spinal neural circuits that underlie swimming, the spinal locomotor network, makes the lamprey an ‘agent‘ capable of generating a behaviour even in absence of sensory inputs. But this does not mean that the lamprey swims as a simple pre-programmed automaton. The lamprey also responds to external events, such as the relative movement in water during the swimming. Such relative water flow is sensed by neurons ending on the surface of the lamprey’s body. In addition, there are sensory neurons located on the surface of the spinal cord4. These two classes of sensory neurons detect the movement produced by the swimming, making the lamprey sensitive to its own swimming movements. Such neural impulses re-enter the spinal cord (‘re-afference‘) affecting the lamprey’s locomotor circuits. These re-entering sensory inputs make the lamprey kind of ‘sentient’.
- See SM Suryanarayana et al (2022): The neural bases of vertebrate motor behaviour through the lens of evolution. Philosophical Transactions of the Royal Society B 377, 20200521.
Sten Grillner & Abdeljabbar El Manira (2020): Current principles of motor control, with special reference to vertebrate locomotion. Physiological Reviews, 100, 271-320.
Sten Grillner (2023): The Brain in Motion – From Microcircuits to Global Brain Function. MIT Press. ↩︎ - GN Orlovksy et al (1999): Swimming in the lamprey. In: Neuronal Control of Locomotion from Mollusc to Man, pp112-147. Oxford University Press. ↩︎
- Sten Grillner & Peter Wallén (2002): Cellular bases of a vertebrate locomotor system – steering, intersegmental and segmental co-ordination and sensory control. Brain Research Reviews 40, 92-106. ↩︎
- J Christenson et al (1988): The dorsal cell, one class of primary sensory neuron in the lamprey spinal cord. I. Touch, pressure but no nociception — a physiological study. Brain Research 440, 1-8. ↩︎