Wolpaw & Tennissen (2001): Activity-dependent plasticity occurs in the spinal cord throughout life

[Wise Young]

• Wolpaw JR and Tennissen AM (2001). Activity-dependent spinal cord plasticity in health and disease. Annu Rev Neurosci. 24: 807-43. Summary: Activity-dependent plasticity occurs in the spinal cord throughout life. Driven by input from the periphery and the brain, this plasticity plays an important role in the acquisition and maintenance of motor skills and in the effects of spinal cord injury and other central nervous system disorders. The responses of the isolated spinal cord to sensory input display sensitization, long-term potentiation, and related phenomena that contribute to chronic pain syndromes; they can also be modified by both classical and operant conditioning protocols. In animals with transected spinal cords and in humans with spinal cord injuries, treadmill training gradually modifies the spinal cord so as to improve performance. These adaptations by the isolated spinal cord are specific to the training regimen and underlie new approaches to restoring function after spinal cord injury. Descending inputs from the brain that occur during normal development, as a result of supraspinal trauma, and during skill acquisition change the spinal cord. The early development of adult spinal cord reflex patterns is driven by descending activity; disorders that disrupt descending activity later in life gradually change spinal cord reflexes. Athletic training, such as that undertaken by ballet dancers, is associated with gradual alterations in spinal reflexes that appear to contribute to skill acquisition. Operant conditioning protocols in animals and humans can produce comparable reflex changes and are associated with functional and structural plasticity in the spinal cord, including changes in motoneuron firing threshold and axonal conduction velocity, and in synaptic terminals on motoneurons. The corticospinal tract has a key role in producing this plasticity. Behavioral changes produced by practice or injury reflect the combination of plasticity at multiple spinal cord and supraspinal sites. Plasticity at multiple sites is both necessary-to insure continued performance of previously acquired behaviors-and inevitable-due to the ubiquity of the capacity for activity-dependent plasticity in the central nervous system. Appropriate induction and guidance of activity-dependent plasticity in the spinal cord is an essential component of new therapeutic approaches aimed at maximizing function after spinal cord injury or restoring function to a newly regenerated spinal cord. Because plasticity in the spinal cord contributes to skill acquisition and because the spinal cord is relatively simple and accessible, this plasticity is a logical and practical starting point for studying the acquisition and maintenance of skilled behaviors. <http://www.ncbi.nlm.nih.gov/htbin-post/Entrez/query?db=m&form=6&dopt=r&uid=11520919
http://neuro.annualreviews.org/cgi/content/full/24/1/807
http://neuro.annualreviews.org/cgi/content/abstract/24/1/807> Laboratory of Nervous System Disorders, Wadsworth Center, New York State Department of Health and State University of New York, Albany, New York 12201-0509, USA. wolpaw@wadsworth.org

[This message was edited by Wise Young on September 23, 2001 at 10:30 PM.]

[Wise Young]

Jonathan Wolpaw has long championed the idea that the spinal cord has the capability to learn even without any brain inputs. This is quite a novel concept 10 or more years ago because the spinal cord was considered to be a "dumb" organ. Yes, it was equipped with reflexes and a number of other circuits that were necessary for specific types of function such as locomotion. There were already the inkling of ideas that there was a locomotor generator system in the spinal cord that is programmed to perform the various types of activities of walking, running, jumping, etc. But, most of the data reporting the presence of such central pattern generators were obtained from primitive animals such as the lamprey and these centers were thought to be "hard-wired".

About a decade or so ago, Wolpaw showed that the lower spinal cord, transected so that it cannot communicate with the brain, is capable of learning. He used classical and operant conditioning techniques (classical means association with noxious stimulation or pleasant stimulation while operant is reward based behavioral training). In any case, he showed that the spinal cord was not only capable to learning and being trained, he found that it had a memory of sorts.

In the last few years, this concept has been expanded to include the ability of the isolated spinal cord to learn specific motor behaviors in response to the environment, that such learning can occur quickly and also last quite some time. This was the work of Reggie Edgarton at UCLA. Conceptually, this is really very interesting because it explains why treadmill training of the spinal cord does produce significant improvements in locomotor behavior of rats even without any connection of the lower spinal cord to the the brain.

Wolpaw makes a strong case that plasticity is present in the spinal cord and that it is present even in adults. Many early investigators suggested that plasticity was really a developmental trait and that when the animal becomes an adult, the degree of plasticity of the system declines. This and the finding that learned non-use plays a role in loss of function, and that forced use training can result in recovery of voluntary locomotor recovery in as many as 40% of people who have never walked after injury, combine to suggest that we need a different rehabilitation approach to spinal cord injury. It will revolutionize rehabilitation as we know it today. It also has important implications for the need for rehabilitation associated with regenerative therapies of spinal cord injury.

Wise.