Endurance exercise, tryptophan availability to the brain, and sleep electrophysiology in older men

Abstract

Normal aging entails significant changes in serotonergic activity and function. Noteworthy, these alterations might predispose older individuals to develop depressive symptoms and contribute to age-related changes in sleep. This study verified if exercise increases tryptophan (Trp) availability to the brain and affects sleep depth and architecture in older men. Nineteen men (aged 64 ± 3 years) undertook a series of 4 tests, which was repeated at follow-up (after 16 weeks of training) as follows: (i) dual-energy X-ray absorptiometry (body composition); (ii) peak O2 consumption, ventilatory threshold, and respiratory compensation point (cardiopulmonary testing); (iii) blood withdrawals immediately before, during, and after exercise for analysis of glucose, lactate, ammonia, free fatty acids (FFA), total proteins, albumin, prolactin, valine, leucine, isoleucine, adiponectin, leptin, free and total Trp, and calculated variable: branched-chain amino acids (BCAA); and (iv) sleep electrophysiology (wake, stage 1, stage 2, stages 3+4 or slow-wave sleep (SWS), stage 5 or rapid eye movements, movement time, leg movements during sleep, apneas, hypopneas, and derivative variables). The intervention consisted of supervised exercise (3× per week × 45 min, 65%–70% peak oxygen uptake (V̇O2peak) whereas experimental exercise consisted of 1 h of inclined treadmill (∼68% V̇O2peak). Variations in serum prolactin and free Trp/BCAA served as proxies of 5-hydroxytryptamine activity and synthesis rate, respectively. A series of 3 nights was assessed before and after training using laboratory-based sleep electrophysiology (polysomnography: electroelectroencephalography and electromyography and electro-oculography) as follows: (i) familiarization, (ii) inactive trial, and (iii) exercise trial. Aerobic taining increased oxygen uptake at both ventilatory thresholds, whereas body mass decreased. Acute exercise increased free Trp/BCAA ratio by more than 100% of that at rest and remained elevated postexercise. This ratio shared a positive association with FFA levels. After 1 h of exercise, prolactin was higher than that at rest and was positively associated with free Trp/BCAA. However, the acute response to exercise was attenuated following training for many compounds, including free Trp/BCAA, prolactin, lactate, and FFA. Analyses revealed significant main effects of exercise on wake after sleep onset, rapid eye movement onset latency, and time awake overnight. As compared with the inactive trial at baseline, a higher proportion of SWS was observed during the night subsequent to exercise following training. In addition, we found a positive association between resting adiponectin and SWS. The results support the hypothesis that increases in serotonin synthesis and activity might be involved in the antidepressant outcome of exercise in older men. Inasmuch as training lowered the increase in Trp supply during exercise, Trp requirement by the brain in response to exercise might be attenuated by training. Despite gains in cardiorespiratory fitness after training, a day without exercise led to SWS values similar to those at baseline. However, exercise increased the proportion of SWS during subsequent sleep but this could only be found after training. These results provide evidence that not only sleep quantity (duration) but also quality (SWS) could affect circulating adiponectin levels. Finally, a positive correlation was found between sleep depth and circulating adiponectin levels.