These spinal networks were made for walking

The invasion of the land by animals was an astonishing evolutionary feat, necessitating a number of substantial changes to the body: limbs with digits, structures for obtaining oxygen from the air, a relatively waterproof covering to prevent dehydration, and sturdy structures to support the body in a medium much less buoyant than water, to name a few. When these pilgrims first bridged the immense gulf between land and water, almost every system in the vertebrate body underwent substantial modifications, but what about the nervous system?

The different optical and sound properties of water and air required significant adaptations for our visual and auditory systems, but these adaptations were largely peripheral: the lens changed shape to adapt to the different refractive indices, and the bones of the middle ear evolved from other bones of the face. Perhaps the most significant behavioral modification (which would thus require notable rewiring of the neural circuitry) was the transition from swimming to walking. Did animals need to invent completely new pathways to support a wider repertoire of locomotion?

First, it's necessary to have a general understanding of the neural basis of locomotion: central pattern generators (CPGs). I posted on CPGs a little while ago; the basic idea is they are networks of neurons, located in the spinal cord, which coordinate all of the muscles involved in locomotion without input from the brain. I focused on bipedal motion, but CPGs control rhythmic locomotory movements in all vertebrates, including those that swim and fly. Thus a more focused question is: when animals transitioned from swimming to walking, could the same CPGs that controlled aquatic locomotion handle the different coordination needed between a body and its limbs for walking?

An excellent paper was published today in Science that explored this question using a robotic salamander (named Salamander robotica because scientists are pretty bad at naming things). Salamanders are considered to be the most similar to the first terrestrial vertebrates, and are thus often used as a model system for studying the evolution of new anatomical structures for terrestrial (vs aquatic) locomotion.

Salamanders can rapidly switch from swimming (using undulations similar to those of primitive fish), to walking (using diagonally-opposed limbs that move together while the body forms an S-shape, like an alligator). Looking at the animal's movements from above, the body can be seen as either moving in a traveling wave or a standing wave, respectively, and neural activity along the spinal cord is likely to mirror this effect.

The group, led by physicist Auke Jan Ijspeert and neurobiologist Jean-Marie Cabelguen, designed Salamander robotica with an electronic "spinal cord" to determine whether the same spinal network could produce both swimming and stepping patterns, and how it might transition between the two.

Their spinal cord was controlled by an algorithm that incorporated essential known or speculated attributes of salamander locomotion. First, the group knew (from a study they did in 2003) that the transition between standing and traveling waveforms can be elicited simply by changing the strength of the excitatory drive from a specific region of the brainstem. In this experiment, a weak drive induced the slow, standing wave of the walking gait, while a stronger drive induced the traveling wave of the swimming motion. Second, the authors reasoned that there are two fundamental CPGs controlling salamander locomotion: the body CPG, located along the spinal cord, and the limb CPG, located at each of the limbs.

With these parameters in place, Salamander robotica set forth on her quest to traverse land and sea, to test whether her "primitive" swimming circuit (the body CPG) would be able to coordinate with the "newer" circuits of her phylogenically recent limbs to produce the waddling gait of her sentient inspiration. Watch the results:

So mechanistically, how does she do it? The group found that at low frequencies, both CPGs are active; the limbs then alternate appropriately, and are coordinated with the movements of the body. At higher frequencies, the limb CPGs are overwhelmed, and thus the limbs tuck in as the body CPGs take over.

One interpretation here is that the group is good at building robots, so Salamander robotica did exactly what they wanted it to do. Another interpretation, the one that got this study into Science and into my blog (quite selective, really), is that the spinal locomotor network controlling trunk movements has remained essentially unchanged during the evolutionary transition from aquatic to terrestrial locomotion.

I think this experiment was highly innovative. As you might imagine, it is quite difficult to study evolution in a controlled laboratory setting (global warming suffers from similar drawbacks, but that's a whole 'nother post), so using robotics as an experimental model is quite promising. The core finding, however, was not surprising to me.

The transition from water to land necessitated a daunting number of anatomical changes and, looking back 370 million years, it seems an unsurmountable divide. But the success of evolution hinges on the fact that it occurs gradually, and rarely involves unusual or extraordinary biological processes. It is thus logical that a common, underlying neural mechanism for propulsion can produce a variety of movements; we see this in modern humans, as well. As I pointed out in my earlier post, the same CPGs--in fact, the same neurons in the same CPG--are used for walking, running, hopping, and skipping. The fact that locomotion is largely independent of conscious control strengthens this rationale; it is much more straightforward to make small adjustments to the system by tinkering "downstream." Thus, when animals adapted to terrestrial locomotion, they used the most efficient (and thus most likely to be successful) strategy: recruiting the same neural circuits used for aquatic locomotion.

Which is not to say that this finding is any less wonderful. It is simply a powerful reminder that, as evolutionary biologist Neil Shubin wrote, "the ancient world was transformed by ordinary mechanisms of evolution, with genes and biological processes that are still at work, both around us and inside our bodies." This is, in his words, "something sublime."

For more information, The Neurophilosopher has an excellent, more detailed post on this paper.

How a chicken can run around with its head cut off

When's the last time you walked? Most of us, excepting those with disabilities, probably walked relatively recently. Walking is a routine behavior that's very routine, learned at an early age and performed without much mental effort. So a more difficult question: when's the last time you thought about what our bodies do when we walk? If you take the time to consider the behavior, walking is a tremendously complex task.

When we walk, we activate hundreds of muscles in an extremely precise, sequential manner. We need to alternate our legs, alternate our flexors (the muscles that bend a joint, e.g. quads) with our extensors (muscles that straighten a joint, e.g. hamstrings), bend our hip/knee/ankle/foot at the appropriate times, and do all of this with relative fluidity. When neuroscientists initially sought to understand the neural mechanisms underlying walking behavior, one of the major issues was whether it required conscious control.

To explore this issue, there was a pretty easy (if a bit blunt) solution: remove the cortex. So in the early 1900s, there were a number of studies performed in which the cortices of neonatal cats were removed. These "decorticate" cats matured into adults, and were able to stand and walk around. Thus, the researchers concluded that walking does not require descending input from the cortex.

[Importantly, certain other brain structures, such as the basal ganglia, were left intact. Damage to the basal ganglia can result in a phenomenon called "obstinate progresson," which is an amusingly fitting name for the behavior. A cat with severe obstinate progression will walk, and walk, and walk...and walk....even if it walks into a wall, its legs will continue to make walking movements!]

How does this work? There's been a fair bit of progress since the early days of decorticate cats. We now understand that the motor system is arranged in a hierarchy, as illustrated in the figure below. First, we make the decision to start walking (this requires the brain). The brain then gives the command ("start walking") to a different part of the nervous system: a circuit of neurons located in the spinal cord called the "central pattern generator," or CPG. Once activated, the CPG activates the relevant muscles and essentially takes care of all of the details. So that is the general strategy for locomotion: when we decide to walk, our brains "recruit" the appropriate CPG, and this CPG is responsible for activating the appropriate muscles at the appropriate time. And thus, although we consciously decide to start and stop walking, we don't need to think about it in between. Once initiated, the motion persists without cortical input.



[Side note: Precise patterns of muscle contractions aren't just involved in walking, but in all coordinated, rhythmic movements, including swimming, flying, breathing, chewing, even sneezing. (So someone unable to walk and chew gum at the same time has a defective spinal cord, not poor intellectual capacity).]

So the brain's (largely) out of the equation...how does the CPG handle locomotion? As I said, the CPG is a "neural circuit"... just like a computer circuit, a neural circuit has a number of units that communicate with each other to modulate the output (with walking, the output activates specific leg muscles). To simplify things, we can ignore the majority of muscles, such as those controlling the bending of the knee, ankle, and foot (and don't forget about our arms, which are coordinated with our legs when we walk), and think of 4 targets of the CPG output: the right and left hamstring, and the right and left quadricep. The important elements of walking are alternating left and right, and alternating flexor and extensor.

Consider a stride in which your right foot is on the ground and your left hip is bending to make the next step. In this case, the left quad is activated, while the right quad is not, nor is the left hammy. However, the hammy of our "stationary" foot is activated, to help straighten the right hip and propel us forward. So when thinking about the neuronal components underlying these properties, one can imagine that when the motor neuron (which is a neuron that innervates (directly communicates with) a muscle) innervating the left quad is active, the CPG ensures that the motor neurons innervating the right quad and left hammy are inhibited, while the motor neuron activating the right hammy is active.

The walking CPG can be translated to other activities: what about hopping? When we decide to hop, our brain activates the locomotor CPG accordingly. Since we want to move both legs together, the CPG coordinates the output such that the quads are activated together, and the hamstrings are activated together, but neither hamstring is ever activated when a quad is activated. So, you can see that a single circuit that controls the quads and hamstrings is flexible and adaptable.

[In a follow-up post, I'll go into the network logic of the CPG, and speculate how the CPG is able to coordinate the motor neurons with such precision...the knowledge in mammals is far from complete, but there have been some interesting recent studies!]

So, the infrastructure of the motor system is arranged such that the brain doesn't have too much responsibility when it comes to routine, rhythmic behaviors. Once it activates the appropriate spinal cord circuit to take care of the important details, it can move on to more interesting things. And thus, people can drink coffee and read the paper while walking to work, watch Lost and Top Chef while working out on the elliptical trainer, and chickens can run around with their heads cut off.