Getting a Sense of the Sixth Sense

“This “proprioception” is like the eyes of the body, the way the body sees itself.”

– Oliver Sacks in The Man Who Mistook His Wife For A Hat

Think about baseball. Right before the pitcher throws the ball, the ball and his hand are behind him, out of his sight. Yet, he knows where his hand and the ball are and how both are moving. How is this possible? The pitcher can tell where the ball is using his sixth sense. No, this is not the same sixth sense that the character played by Haley Joel Osment has in the movie The Sixth Sense. This sixth sense is known as proprioception (pronunciation: PRO-pree-o-SEP-shən). Proprioception is the sense that allows us to determine the relative position and movement of our body parts in space. So what do we know about proprioception? How does it work?

Image of Charles Sherrington who coined the term

Image of Charles Sherrington who coined the term “proprioception” in 1906 (image from: wikimedia commons)

The word, “proprioception” was coined by the British scientist Charles Sherrington in 1906. Sherrington identified two types of sensory neurons that innervate the muscle that are now known to underlie proprioception. These neurons are known as muscle spindles and Golgi tendon organs. Muscle spindles innervate muscle fibers and detect changes in muscle length while Golgi tendon organs innervate the junction between muscles and detect changes in muscle tone (the effort exerted by muscle). Unlike the other five senses, proprioception does not have a designated sensory organ; rather information is collected from the whole body. This information is sent up through the spinal cord to the cerebellum where the positions of body parts in space are calculated.

While the neurons involved in proprioception have long been identified, the molecular mechanisms underlying this sense are just beginning to be understood. In a recent paper, Woo et. al (2015) identify the mechanoreceptor Piezo2 as a mechanically-gated ion channel involved in translating muscle movement to electrical signals that are then transmitted to the central nervous system. When a muscle moves, the membrane of the neurons innervating it also moves, creating a mechanical force that opens these ion channels, allowing positively charged ions to flow into the neuron and thus creating an electrical impulse.

The muscle spindle and Golgi tendon organ are the proprioreceptors that detect and transmit changes in muscle length and tone to the rest of the nervous system (image source: http://www.medicalook.com/human_anatomy/organs/Proprioceptors.html)

The muscle spindle and Golgi tendon organ are the proprioreceptors that detect and transmit changes in muscle length and tone to the rest of the nervous system (image source: http://www.medicalook.com/human_anatomy/organs/Proprioceptors.html)

The first evidence for Piezo2’s involvement in proprioception was its strong expression on muscle spindles and Golgi tendon organs in mice. The authors also demonstrate that the electrophysiological response properties of these neurons in response to mechanical stimulation resemble that of cells expressing the Piezo2 channel alone. Finally, the authors show that mice lacking Piezo2 in the proprioceptive neurons (conditional knockout mice) have severely impaired limb coordination, suggesting that Piezo2 is necessary for proprioception. [1] These findings have opened the door for scientists to further understand the molecular mechanisms that give rise to proprioception within the muscle spindles and Golgi tendon organs. However, it has to be noted that there is a lot more to proprioception beyond these two neuronal groups.

Longo and Haggard (2010) argue that while the cerebellum receives information on muscle stretch and tone from proprioceptive neurons, this information on its own is insufficient for the person to know where his body is in space. Information such as body size and shape are also crucial for this process. Longo and Haggard hypothesize that there must be a “stored body model” that the brain learns over time and is used as a reference map for information such as the length of your arm. [2] It is also suggested that the development of this map includes information not just from the proprioceptive neurons but also from other senses, primarily vision. [3] This could explain why a child learning the piano for the first time needs to look at his fingers to make sure he hits the right notes. However, a master pianist can play blindfolded and still know exactly where each finger is relative to the other.

Proprioception, the sixth sense, is a critical one. It enables many of the daily actions that we do without thinking. A loss of this proprioceptive sense is almost unimaginable to many of us, but it does happen. Damage to the nerves from injury or infection can lead to loss of this sense; affected people are unable to tell where their body parts are when they cannot see them (Ian Waterman is one such person). Therefore, developing a better understanding of how proprioception works and what the mechanisms involved are is vital. So, how are visual and proprioceptive inputs assimilated to create this “stored body model”? How do the molecular mechanisms underlying proprioception change as we develop this mental map of our body or as we learn to play the piano? Is Piezo2 expression or function involved in this? It will be interesting to see these questions answered as we get a better sense of proprioception.

Reference:

  1. Woo, S-H., Lukacs, V., de Nooij, J.C., Zaytseva, D., Criddle, C.R., Francisco, A., Jessel, T.M., Wilkinson, K.A., Patapoutian, A. (2015) Piezo2 is the principal mechanotransduction channel for proprioception Nature Neuroscience
  2. Longo, M.R., Haggard, P. (2010) An implicit body representation underlying human position sense PNAS Vol. 107, No. 26
  3. Blanke, O., Slater, M., Serino, A. (2015) Behavioral, neural and computational principles of bodily self-consciousness Neuron Vol. 88
  4. http://www.hhmi.org/biointeractive/ian-waterman-compensating-proprioceptive-loss
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