CSEP member contributions to the understanding of exercise physiology: a focus on exercise neuroscience

February 8, 2017

The Canadian Society for Exercise Physiology will be celebrating its 50th anniversary in 2017. A signature initiative is a celebration of the contributions of Canadian researchers to exercise physiology over the past 50 years. The objective is to highlight significant Canadian contributors and their contributions to exercise physiology, health and fitness, nutrition and gold standard publications globally as well as provide insights on future research directions in these areas. These achievements have been organized into a series of short historical communiqués on prominent Canadian contributors and will be published on a monthly basis.

CSEP member contributions to the understanding of exercise physiology: a focus on exercise neuroscience

Behm, DG ¹, Gardiner, PF ²*, Garland, SJ ³, Kalmar, JM ⁴, Rice CL ⁵, Shoemaker, JK ⁶, Zehr EP⁷.
¹ School of Human Kinetics & Recreation, Memorial University of Newfoundland
² Faculty of Kinesiology & Recreation Management, University of Manitoba
³ Faculty of Health Sciences, Western University
⁴ Kinesiology & Physical Education, Faculty of Science, Wilfred Laurier University
⁵ School of Kinesiology, Faculty of Health Sciences, Western University
⁶ School of Kinesiology, Faculty of Health Sciences, Western University
⁷ School of Exercise Science, University of Victoria

*To whom correspondence should be addressed:
Phillip Gardiner, PhD
Spinal Cord Research Center,
Basic Medical Sciences Building, Rm 404,
745 Bannatyne Avenue,
University of Manitoba,
Winnipeg MB R3E 0J9
Tel: (204) 977-5622
Email: phil@scrc.umanitoba.ca

Several CSEP members have contributed significantly to our knowledge in the field of exercise neuroscience since the 1970’s. In this short document we have tried to provide a brief description of the activities of members who have been consistently active in the field over a period of several decades, while mentioning the trail of talented trainees that have benefitted from the experience of training in these labs, and have gone on to continue conducting exercise neuroscience research in their own labs.

Dr. Digby Sale

Dr. Digby Sale was an internationally acclaimed leader in the investigations of neuromuscular adaptations associated with resistance training. His career at McMaster University from the 1970s to the 21st century produced extensive information on motor unit and muscle activation with various aspects of strength and power training across the population spectrum. Contrary to the popular myths against resistance training for children, Dr. Sale with other luminaries such as Dr. Duncan MacDougall, Dr. Oded Bar-Or and Dr. Cameron Joseph Blimkie demonstrated the positive neuromuscular and muscular adaptations with youth. Digby also studied resistance training with elderly in articles with Dr. Neil McCartney and Dr. Audrey Hicks. His work on the velocity specificity of resistance training was the first to demonstrate that the intent (cortical command) to contract explosively was a more important factor than movement speed, which had been a foundation of velocity specificity for 20 years. His work with his graduate student Paul Zehr examined neuromuscular adaptations with high-speed ballistic training detailing the extent, timing and specific muscle contributions of agonist and antagonist muscle activation. The resistance training variables he examined over his career are too many to discuss within one paragraph (e.g. neural potentiation, bilateral deficits, occlusion training, accommodating loads, whole versus split resistance training routines, and others). His reviews on neuromuscular adaptations to resistance and strength training are among the most highly cited in the area. Even during retirement, he is still contributing to the area with a textbook (Physiology of Training for High Performance with Dr. MacDougall as co-author) released in 2014. Trainees with Dr. Sale who continue related work in exercise neuroscience include David Behm (Memorial), Paul Zehr (Victoria), and Philip Chilibeck (Saskatchewan).

Dr. Phillip Gardiner

Since the 1980’s, Dr. Phillip Gardiner has focussed his research on the plasticity of the nervous and neuromuscular systems in response to increased and decreased physical activity, aging, and trauma (spinal cord injury). In a unique research program initiated at Université de Montréal, and later as a tier I CIHR Canada Research Chair at University of Manitoba (since 2002), Dr. Gardiner demonstrated plasticity at several levels of the neuromuscular system, including the neuromuscular junction, the motor unit, and the motoneuron, using animal models. For example, the Gardiner laboratory was the first to demonstrate that chronic physical activity/inactivity has profound effects on the basic biophysical properties of spinal motoneurons that would influence how these neurons respond to excitatory and inhibitory signals. His lab also demonstrated changes in gene expression in motoneurons that could explain some of these biophysical changes. Ongoing work in the Spinal Cord Research Centre at University of Manitoba, of which Dr. Gardiner is currently Director, focusses on the effects of spinal cord injury, as well as activity-related plasticity in sensory neurons and the spinal circuits involved in locomotor activity. Dr. Gardiner published two books in the area: Neuromuscular Aspects of Physical Activity (2001), and Advanced Neuromuscular Exercise Physiology (2012). Trainees that have spent time in the Gardiner lab and are currently continuing exercise neuroscience-related research include Robin Michel (Concordia), Bernard Jasmin (Ottawa), Reza Gharakhanlou (Tehran), Bruno Cormery (Pau, France), Eric Beaumont (Tennessee), Tanguy Marqueste (Marseilles, France), Duane Button (Memorial), Kevin Power (Memorial), Jayne Kalmar (Wilfred Laurier), Jeremy Chopek (Dalhousie), Claudia Verret (UQAM), and Chris MacDonell (Manitoba).

Dr. Enzo Cafarelli

Dr. Enzo Cafarelli investigated acute and chronic adaptations of the neuromuscular system, contributing significantly to our understanding of the central and peripheral inputs that alter human motor unit behavior and the voluntary activation of muscle. Over the course of his career at York University from 1977 to 2007 (Emeritus 2007-2016), Dr. Cafarelli’s work has identified neuromuscular adaptations to fatigue and resistance training, from motor cortex, to motor unit, to muscle. His group also demonstrated the effects of caffeine on motor unit firing behaviour, contractile function, and force sensation, and used caffeine as a tool to investigate CNS contributions to fatigue. While his primary focus was the neural control of muscle in healthy adults, Dr. Cafarelli also investigated neuromuscular fatigue associated with diabetic myopathy in humans and rodent models. Many of Dr. Cafarelli’s trainees continued on to research careers in neuromuscular and exercise physiology related disciplines including Jennifer Jakobi (UBCO), Lisa Griffin (Texas), Jayne Kalmar (Wilfrid Laurier), and Peter Adhihetty (Florida). In 1995, Dr. Cafarelli formed the Ontario Exercise Neuroscience Group with the intent of bringing a small group of physiologists (including Cafarelli, Garland, Rice, and Gardiner) together with their trainees to discuss a common interest in the neural aspects of exercise physiology in a student-centred conference. The creation of this group, which was intended to foster faculty and trainee interaction in a social environment, best exemplifies Dr. Cafarelli’s passion for the field and his commitment to mentoring future scientists. The group still meets biennially with an attendance that has more than tripled and now includes young investigators from Canada’s east to west coasts that were trained by the founding members of the Exercise Neuroscience Group. The scientists that Enzo united in 1995 to discuss a growing trend have remained a cohesive group that has together mentored a new generation of students and young investigators who are interested in the effects of exercise on the central nervous system.

Dr. S Jayne Garland

Dr. S Jayne Garland has worked in the field of exercise neuroscience since the mid-80s. She was one of a few pioneering physical therapists working in neurophysiology and motor control. Her work has focussed on the neural control of muscle fatigue in healthy participants and in people with a variety of chronic health conditions (stroke, breast cancer, chronic obstructive lung disease, osteoarthritis, renal disease, multiple sclerosis). Although common now, Dr. Garland was among the first researchers who recorded from single motor units during high-force and dynamic contractions, which expanded the relevance and application of motor control findings to activities of daily living. She was also instrumental in advancing the work of PBC Matthews in the modelling of motoneurone afterhyperpolarization in humans. Her work on understanding the postural control mechanisms underlying standing balance culminated in a clinical trial investigating the effects of fast muscle activation and stepping training on community balance in people recently discharged from stroke rehabilitation. Dr. Garland spent the first 20 years of her career at Western University, then was Head of the Department of Physical Therapy at the University of British Columbia from 2009-2015, and returned to Western in 2016 as Dean of the Faculty of Health Sciences. She is one of the founding members of the International Motoneurone Society, which has continued to advance the integration of motoneurone research among scientists using animal and human models. Trainees who have continued in the field of exercise neuroscience include Lisa Griffin (Texas), George Mochizuki (Toronto), Chris MacDonell (Manitoba), and Vicki Gray (Maryland).

Dr. Charles Rice

Dr. Charles Rice focussed his research studies at a systems or integrated level in humans exploring questions related to neuromuscular factors that affect muscle force generation in health, aging, acute (fatigue) and chronic (exercise) states, and some clinical conditions. These adapted states have served as models to help understand key factors and their interrelationships and adaptability between neural drive and muscle properties to achieve purposeful contractile output. Uniquely, he exploited the benefits of the human model by using a comprehensive approach of minimally invasive tools and techniques such as recordings of motor unit firing rates at all force levels (neural output), electrically stimulated and voluntarily controlled neuromuscular responses (neuromuscular and contractile function) and muscle imaging (muscle structure) to gain insights from several key aspects of the system concurrently. Dr. Rice began his research career at McGill University, but has done most of his work over the past ~20 years at The University of Western Ontario. Much of his work has focussed on adult ageing in conjunction with key collaborators Dr. Tony Vandervoort and Dr. Tim Doherty. Notably, studies have revealed the importance of the motor unit in understanding age-related muscle wasting (sarcopenia); originally considered primarily due to factors residing only in the muscle. Advances in understanding age-related fatigability during dynamic contractions and the positive effects on the motor unit of life-long physical activity have been gained from his studies. Uniquely, the lab has been successful with recording motor unit properties during a range of dynamic contraction velocities, intensities and during fatiguing tasks which have provided novel insights – considering that almost all of our understanding of motor unit properties to date has been discovered from isometric conditions. Dr. Rice is currently Research Director at the Canadian Centre for Activity and Aging. Past lab doctoral trainees who are now established exercise neuroscientists include: Jennifer Jakobi (UBCO), Brian Allman (Western), Arthur Cheng (Karolinska Institute), Chris McNeil (UBCO), Brian Dalton (UBCO), and Geoff Power (Guelph).

Dr. E. Paul Zehr

Since his first publications on the physiology of karate, Dr. E. Paul Zehr has focused on various aspects of adaptive plasticity and the neuroscience of human movement. His work begun initially the Human Neurophysiology Laboratory at the University of Alberta and continuing in the Rehabilitation Neuroscience Laboratory at the University of Victoria revealed the integrative role of interlimb linkages in human posture and locomotion. The work from Zehr’s laboratory revealed the short and long term plasticity that arm movement can induce in human lumbar spinal cord reflex networks and the extensive role for somatosensory feedback in regulating spinal cord networks between the arms and legs. This interlimb influence is also found in Zehr’s work in strength training and adaptive reflex plasticity where a clinical application to “cross education” for functional recovery after stroke has been pioneered. Dr. Zehr’s work has answered basic research questions that lead directly to clinical studies with rehabilitative applications such as motor recovery after neurological damage such as occurs after spinal cord injury and stroke. A unique focus of Dr. Zehr’s work is the translation of knowledge about exercise science to the general public using popular culture. His books and science writing use superheroes like Batman, Iron Man, and Batgirl as foils for explaining to the general public the real power of physiological adaptation found within. Trainees or scientists who have passed through the Zehr laboratory who continue related work in exercise neuroscience include Trevor Barss (Alberta), David Collins (Alberta), Alain Frigon (Sherbrooke), Sandra Hundza (Victoria), Marc Klimstra (Victoria), Rinaldo Mezzarane (Brasilia), Tsuyoshi Nakajima (Kyorin University), Aiko Kido Thompson (Medical University of South Carolina), and Erin Vasudevan (Stonybrook).

Dr. Kevin Shoemaker

Since the late 1990s, when Dr. Kevin Shoemaker began publishing observations of the sympathetic nervous system (SNS) and vascular function in humans, he has dedicated his research to understanding the communication strategies used by this nervous system and the interplay between neural and vascular tissue both in the periphery and in the brain. Further, he studies the malleability of this neural system to deconditioning and conditioning stimuli, as well as sex hormones, age and disease. In 2005, he initiated novel programs of research that focused on mapping the cortical autonomic network associated with exercise and other reflex cardiovascular stimuli. For example, his laboratory was the first to map critical sites within the forebrain and midbrain that were associated with autonomic control during exercise and reflex stimuli. Within the context of a Tier 1 Canada Research Chair opportunity, his research focused on structural and functional brain imaging models as well as neural recruitment strategies within the SNS. These studies produced new knowledge regarding the deleterious effects of age and vascular disease on functional cortical autonomic network, showing accelerated brain atrophy with aging in cardiac patients that could be restored with cardiac rehabilitation. He also provided the first direct measures of vasoactivity in cerebral arteries of conscious humans. Concurrently, his laboratory was the first to demonstrate specific recruitment strategies within the sympathetic nervous system of humans, illustrating marked and reproducible patterns of rate coding, recruitment of latent high threshold but fast-conducting action potentials, and variations in synaptic delays. The combined results point to selective cognitive versus reflex stimuli that affect different patterns of sympathetic efferent recruitment. Trainees from Dr. Shoemaker’s laboratory who continue in autonomic, neurovascular and/or cerebrovascular research include Jorge Serrador (Rutgers), Tim Wilson (Western), Derek Kimmerly (Dalhousie), Michel Johnson (New Brunswick), Deborah O’Leary (Brock University), Savio Wong (Hong Kong), Craig Steinback (Alberta), Sophie Lalande (Toledo), Heather Edgell (York), Antti Kiviniemi (Oulu), David Ditor (Brock).

Contributions by these scientists to the legacy of exercise neuroscience in Canada include not only the science that has emanated from their labs but, perhaps more importantly, the continuing contributions of their trainees to this exciting and important field of exercise physiology.

*To whom correspondence should be addressed:
Phillip Gardiner, PhD
Spinal Cord Research Center,
Basic Medical Sciences Building, Rm 404,
745 Bannatyne Avenue,
University of Manitoba,
Winnipeg MB R3E 0J9
Tel: (204) 977-5622
Email: phil@scrc.umanitoba.ca