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05.23 The Wonders of Walking
The Wonders of Walking    
 

Highlights

  • Spinal cord injuries affect over 250,000 people in the United States. There is currently no treatment that can reverse damage done to the spinal cord.

  • A better understanding of the function of the spinal cord may allow for the development of novel treatments for spinal cord injuries. These researchers used the cat model to investigate how the spinal cord controls balance and locomotion.

  • The results of this research will be used to develop computational models of cat locomotion. The researchers hope their findings will be translated into improved clinical care for people with spinal cord injuries.


One of the distinguishing characteristics of the human species is our ability to move around on two—not four—limbs. However, take a closer look at the arms of a human on the move, and you’ll see that they swing in a coordinated pattern. When the right foot goes forward, the left arm moves forward as well.


Figure 1. Human walking sequence recorded by motion capture. Notice how the arms move in coordination with the legs.
[Source: By Lars Lau Raket - Own work, CC BY-SA 4.0,https://commons.wikimedia.org/w/index.php?curid=92854391]


Try to walk without swinging your arms, and you’ll notice that you have to actively use your shoulder muscles to do so. You might also find that your balance is off. This is because the networks of neurons that control our movements are connected to our evolutionary ancestors on four limbs. In fact, this is exactly how cats and dogs coordinate their forelimbs and hindlimbs while in motion, by moving diagonal limbs together in synchrony, a type of gait pattern that is known as a trot.

Understanding how these networks function to allow for movement in space, or locomotion, could open up new pathways for the treatment of people with spinal cord injuries. This is the goal of research conducted by Dr. Alain Frigon, Professor of Neuroscience and Physiology in the Department of Pharmacology-Physiology at the University of Sherbrooke in Quebec, Canada, and a team of international colleagues.

Locomotion and the Nervous System

Locomotion is controlled by the nervous system. The nervous system is composed of the brain, spinal cord, and nerves, which together regulate all other functions in the body. The building blocks of the nervous system are neurons, specialized nerve cells that use electrical activity to transmit messages from the brain to the rest of the body and back.

There are different types of neurons in the body that perform specific functions, many of which remain unknown. Neurons can be broadly grouped into three categories based on their function: interneurons, sensory neurons, and motor neurons. Interneurons are the most common type of neuron that allow for communication between different parts of the nervous system. Sensory neurons receive input from the environment, such as smell, taste, and touch. Motor neurons communicate messages to muscles, making them contract to generate both voluntary movements like walking and involuntary movements like those involved in digestion.


Figure 2. Example of communication between interneurons (relay neurons) in the spinal cord, sensory neurons, and motor neurons. Sensory neurons communicate to the interneurons that there is a pin in the animal’s paw, and the interneurons direct the motor neurons to respond.
[Source: Ruth Lawson Otago Polytechnic CC BY 3.0.https://commons.wikimedia.org/w/index.php?curid=8831185]


The spinal cord is at the core of locomotion, containing all motor neurons that directly control muscles of the limbs and trunk.


Figure 3. Human spinal cord, labeled according to the position of the vertebrae.
[Source: https://en.wikipedia.org/wiki/Back_pain]


Within the spinal cord, there are networks of interneurons that work together to form neural circuits called central pattern generators that generate rhythmic patterns including patterns of locomotion, known as gait. The central pattern generator signals the motor neurons to activate and contract the relevant muscle fibers in specific parts of the gait cycle. For example, muscles that lift the foot by flexing the different joints need to be activated to swing a leg forward (swing phase, see below). When the foot lands on the ground, muscles must be contracted to resist the force of gravity before propelling the body forward (stance phase, see below). At the same time, the brain needs to make sure that the left and right legs are coordinated together with the arms. All these muscle activations produce a gait pattern that is orchestrated in large part by central pattern generators. This is why walking is largely involuntary and automatic, such that we do not need to think about the movement to produce it.


Figure 4. Central pattern generator (CPG) neurons produce a rhythmic gait by communicating with motor neurons and responding to feedback sensory neurons (dorsal root ganglia and peripheral afferents).
[Source: Dr. Frigon]


When movement begins, sensory neurons in the skin and muscles provide feedback to the motor neurons and interneurons. The brain uses this information to make decisions and tell the central pattern generators in the spinal cord what to do. For example, to change direction or to go faster, based on specific goals and sensory information from the muscles and skin. The central pattern generator is a network of neurons that can produce its own rhythm without receiving inputs from the brain or sensory feedback from the limbs. Scientists hypothesize that one central pattern generator controls each limb and that the central pattern generators communicate with each other through interneurons in the spinal cord.

The human gait cycle, controlled by central pattern generators, is divided into two phases: the stance phase and the swing phase. During the stance phase, the foot remains in contact with the ground; during the swing phase the foot is not in contact with the ground. When one foot is in the stance phase, the other foot begins its swing phase. One gait cycle is defined as the period beginning when one foot touches the ground and ending when that same foot touches the ground again. There are times of double support during the gait cycle when both feet are in stance phase. This is how locomotion works in people with healthy spinal cords.


Figure 5. Phases of the human gait cycle.
[Source: https://commons.wikimedia.org/wiki/File:Walk_cycle.jpg]


Spinal Cord Injuries

In people with spinal cord injuries, communication between neurons in the spinal cord is impaired. For example, the brain may have difficulty sending signals to the spinal cord, or sensory feedback from the limbs may not get communicated properly to the brain. Depending on where the spinal cord injury is located, it can have a variety of effects ranging from decreased motor function and loss of sensation to paralysis of some or all limbs. A major challenge for people with spinal cord injuries is maintaining balance, which requires signals from the brain to the spinal cord as well as sensory feedback from the limbs and trunk to the spinal cord and brain. This signaling is disrupted by spinal cord injury.

The National Spinal Cord Injury Statistical Center estimates that there are currently over 250,000 people in the United States living with spinal cord injuries, and that over 17,000 people acquire spinal cord injuries each year. Motor vehicle accidents are the leading causes of spinal cord injuries in the United States, making up half of all cases of spinal cord injury, according to the American Association of Neurological Surgeons. Other causes include falls, violence, and diseases that affect the nervous system. Depending on the type and severity of spinal cord injury, surgery, medications, and rehabilitation therapy can help some patients. Some recovery of movement and other functions is possible depending on the severity of the injury. However, there is currently no treatment that can reverse the physical damage done to the spinal cord.

Cat Locomotion

Dr. Alain Frigon has focused his research on improving our understanding of the mechanisms underlying the control of locomotion. His ultimate goal is to facilitate the ability of people with spinal cord injuries to walk and maintain their balance.

In his research, Dr. Frigon uses the cat as a model of locomotion because the organization of the spinal cord in humans and cats is similar. This allows for the results of Dr. Frigon’s research in the cat model to more readily be applied to humans. The cats in Dr. Frigon’s laboratory participate in a variety of experiments related to locomotion, including walking on a treadmill, walking on a circular pathway, and walking along a path with obstacles.


Figure 6. Video of a cat walking on a treadmill in Dr. Frigon’s laboratory.
[Source: Dr. Frigon]


In a recent series of experiments, Dr. Frigon and colleagues wanted to better understand how cats respond to obstacles in their path. If a paw unexpectedly hits an obstacle, a cat (or a human) will usually not fall over. Instead, the other limbs will compensate for the instability in the affected limb. “We know that this process of compensating to maintain balance is in part controlled by the spinal cord with feedback from sensory neurons,” explained Dr. Frigon, “but we don’t really know how this happens.”

To investigate, the researchers stimulated the muscles in the cat’s paw while it walked, making the cat feel as if it had just encountered an obstacle. They recorded the electrical activity of muscles in all four limbs at different points in the gait cycle and used the electrical recordings to quantify muscle responses.

The researchers found significant differences in the coordinated response to the stimulated paw depending on where in the gait cycle the stimulation occurred. Increased muscle activity was noted when the stimulated paw was in the swing phase and in transitions between phases. The feedback the cat received from sensory neurons helped it maintain its balance and coordinate its movement, even when confronted with an obstacle. “Our findings contribute to our understanding of how motor neurons, sensory neurons, and interneurons work together to move our body forward while maintaining balance. We are currently performing similar work following spinal cord injuries," explained Dr. Frigon.

Collaborations and Future Research

Dr. Frigon works closely with collaborators Dr. Boris Prilutsky at Georgia Tech University in Atlanta, Georgia and Dr. Ilya Rybak at Drexel University in Philadelphia, Pennsylvania who utilize his research findings to develop computational models of cat locomotion. The researchers hypothesize that these models will show how the cats’ muscles and sensory feedback work with the spinal cord to control and coordinate movement. He also collaborates with Dr. Christian Iorio-Morin, neurosurgeon at the University of Sherbrooke, to develop strategies to electrically stimulate the spinal cord. In the future, the researchers hope these findings can be translated into clinical care for people with spinal cord injuries.

Dr. Alain Frigon is Professor of Neuroscience and Physiology in the Department of Pharmacology-Physiology at the University of Sherbrooke in Quebec, Canada. His research focuses on using the cat model to better understand locomotion with the ultimate goal of helping people with spinal cord injuries. When not in the laboratory, Dr. Frigon enjoys hiking, skiing, cooking, playing video games, and spending time with his family.

For More Information:

  1. Merlet, A. et al. 2022. “Sensory Perturbations from Hindlimb Cutaneous Afferents Generate Coordinated Functional Responses in All Four Limbs during Locomotion in Intact Cats.” eNeuro, 9(6): 0178-22. https://www.eneuro.org/content/9/6/ENEURO.0178-22.2022.full
  2. Harnie, J. et al. 2021. “The Spinal Control of Backward Locomotion.” Journal of Neuroscience, 41(4): 630-47. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7842752/
  3. Frigon, A. et al. 2017. “Left-right coordination from simple to extreme conditions during split-belt locomotion in the chronic spinal adult cat.” Journal of Physiology, 595(1): 341-361. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5199742/
  4. Frigon, A. 2017. “The neural control of interlimb coordination during mammalian locomotion.” Journal of Neurophysiology, 117(6): 2224-41. https://pubmed.ncbi.nlm.nih.gov/28298308/

To Learn More:

  1. Frigon Lab. www.frigonlab.com

  2. National Institute of Neurological Disorders and Stroke. https://www.ninds.nih.gov/health-information/disorders/spinal-cord-injury

  3. American Association of Neurological Surgeons. https://www.aans.org/en/Patients/Neurosurgical-Conditions-and-Treatments/Spinal-Cord-Injury

  4. Shepherd Center. https://www.shepherd.org/patient-programs/spinal-cord-injury/levels-and-types

  5. Understanding Spinal Cord Injury Video Series. https://www.spinalinjury101.org/

Written by Rebecca Kranz with Andrea Gwosdow, PhD at www.gwosdow.com


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