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.