Spinal cord injury-induced changes in breathing are not due to supraspinal plasticity in turtles (Pseudemys scripta)

Abstract

Johnson, Stephen M., and Robert J. Creighton. Spinal cord injury-induced changes in breathing are not due to supraspinal plasticity in turtles (Pseudemys scripta). Am J Physiol Regul Integr Comp Physiol 289: R1550 -R1561, 2005. First published August 11, 2005; doi:10.1152/ajpregu.00397.2005-After occurrence of spinal cord injury, it is not known whether the respiratory rhythm generator undergoes plasticity to compensate for respiratory insufficiency. To test this hypothesis, respiratory variables were measured in adult semiaquatic turtles using a pneumotachograph attached to a breathing chamber on a water-filled tank. Turtles breathed room air (2 h) before being challenged with two consecutive 2-h bouts of hypercapnia (2 and 6% CO 2 or 4 and 8% CO2). Turtles were spinalized at dorsal segments D8-D10 so that only pectoral girdle movement was used for breathing. Measurements were repeated at 4 and 8 wk postinjury. For turtles breathing room air, breathing frequency, tidal volume, and ventilation were not altered by spinalization; single-breath (singlet) frequency increased sevenfold. Spinalized turtles breathing 6 -8% CO 2 had lower ventilation due to decreased frequency and tidal volume, episodic breathing (breaths/episode) was reduced, and singlet breathing was increased sevenfold. Respiratory variables in sham-operated turtles were unaltered by surgery. Isolated brain stems from control, spinalized, and sham turtles produced similar respiratory motor output and responded the same to increased bath pH. Thus spinalized turtles compensated for pelvic girdle loss while breathing room air but were unable to compensate during hypercapnic challenges. Because isolated brain stems from control and spinalized turtles had similar respiratory motor output and chemosensitivity, breathing changes in spinalized turtles in vivo were probably not due to plasticity within the respiratory rhythm generator. Instead, caudal spinal cord damage probably disrupts spinobulbar pathways that are necessary for normal breathing.control of breathing; respiration; reptile; chelonian; episodic breathing IN RESPONSE TO INJURY, THE central nervous system undergoes morphological and physiological changes to compensate for loss of function, such as altered gene expression, neuronal reorganization, and altered synaptic plasticity. Likewise, after incomplete spinal cord injury, remaining descending spinal pathways and spinal motor networks undergo reorganization and neuroplasticity to compensate for loss of function (6,20,51). Because respiratory dysfunction is the leading cause of death in spinal cord-injured patients (9, 59), understanding the mechanisms by which the respiratory control system undergoes compensatory plasticity may lead to novel therapeutic strategies for reducing respiratory complications and subsequent morbidity.After spinal cord injury, breathing pattern is altered to maintain adequate ventilation (V E). For example, high cervical spinal cord injury compromises synaptic drive to phrenic and intercostal motoneurons in mammals, r...

Inhibitory and excitatory effects of μ-, δ-, and κ-opioid receptor activation on breathing in awake turtles,Trachemys scripta

“…These plots showed that expiratory area measurements were relatively insensitive to frequency, with a maximum of 10 -20% error in V E and VT measurements only at the highest VT and frequencies in turtles. Since baseline breathing measurements in the present study were similar to those previously reported (9,19,20,30) and most drugs decreased breathing frequency and increased breath duration, the impact of systematic pneumotachograph errors was deemed to be minimal with respect to the major findings. hydrate (U-50488) were purchased from Sigma-Aldrich (St. Louis, MO).…”

“…Finally, since MOR and DOR activation decreased V E in turtles by decreasing breathing frequency, these turtles would be expected to become hypercapnic and increase VT as a result of increased chemoreceptor drive (20). However, the lack of a significant increase in VT following injection with MOR and DOR agonists suggests that chemoreceptor drive may also have been attenuated, similar to observations in mammals (for review see Ref.…”

5-HT3 receptor-dependent modulation of respiratory burst frequency, regularity, and episodicity in isolated adult turtle brainstems

“…Variability in the degree of endogenous 5-HT 3 receptor activation would account for the differences in baseline episodicity in isolated turtle brainstems; i.e. , 25% of brainstems produce episodic discharge (>2.0 bursts/episode) while 56% of brainstems produce singlet discharge (<1.25 bursts/episode; Johnson and Creighton, 2005). …”

“…Likewise, the terrestrial tortoise ( Testudo graeca ) exhibits both singlet and episodic breathing, but the singlet breathing pattern is dominant (Gans and Hughes, 1967). For intact, semi-aquatic, red-eared slider turtles ( Trachemys scripta ) placed in water-filled tanks, the breathing pattern is mostly episodic with occasional singlets (Johnson and Creighton, 2005; Sladky et al , 2007; Johnson et al , 2008). To our knowledge, the breathing pattern of any chelonian on land versus in water has not been systematically studied, nor is it known whether 5-HT 3 receptor activation modulates breathing pattern in terrestrial or aquatic chelonians.…”

The impact of spinal cord injury on breathing during sleep

“…There has been a limited amount of work in this area, but in our opinion, the literature supports the hypothesis that changes in brainstem respiratory neurons and networks are likely to occur after SCI (Johnson and Creighton, 2005). For example, Golder and colleagues showed that inspiratory motor drive to the tongue is altered following high cervical SCI in rats (Golder et al, 2001).…”