Identifying the role of group III/IV muscle afferents in the carotid baroreflex control of mean arterial pressure and heart rate during exercise

Abstract

Key points: We investigated the contribution of group III/IV muscle afferents to carotid baroreflex resetting during electrically evoked (no central command) and voluntary (requiring central command) isometric knee extension exercise. Lumbar intrathecal fentanyl was used to attenuate the central projection of μ-opioid receptor-sensitive group III/IV leg muscle afferent feedback. Spontaneous carotid baroreflex control was assessed by loading and unloading the carotid baroreceptors with a variable pressure neck chamber. Group III/IV muscle afferents did not influence spontaneous carotid baroreflex responsiveness at rest or during exercise. Afferent feedback accounted for at least 50% of the exercise-induced increase in the carotid baroreflex blood pressure and heart rate operating points, adjustments that are critical for an appropriate cardiovascular response to exercise. These findings suggest that group III/IV muscle afferent feedback is, independent of central command, critical for the resetting of the carotid baroreflex blood pressure and heart rate operating points, but not for spontaneous baroreflex responsiveness.

Abstract: This study sought to comprehensively investigate the role of metabolically and mechanically sensitive group III/IV muscle afferents in carotid baroreflex responsiveness and resetting during both electrically evoked (EVO, no central command) and voluntary (VOL, requiring central command) isometric single-leg knee-extension (15% of maximal voluntary contraction; MVC) exercise. Participants (n = 8) were studied under control conditions (CTRL) and following lumbar intrathecal fentanyl injection (FENT) to inhibit μ-opioid receptor-sensitive lower limb muscle afferents. Spontaneous carotid baroreflex control of mean arterial pressure (MAP) and heart rate (HR) were assessed following rapid 5 s pulses of neck pressure (NP, +40 mmHg) or suction (NS, -60 mmHg). Resting MAP (87 ± 10 mmHg) and HR (70 ± 8 bpm) were similar between CTRL and FENT conditions (P > 0.4). In terms of spontaneous carotid baroreflex responsiveness, FENT did not alter the change in MAP or HR responses to NP (+13 ± 5 mmHg, P = 0.85; +9 ± 3 bpm; P = 0.99) or NS (-13 ± 5 mmHg, P = 0.99; -24 ± 11 bpm; P = 0.49) at rest or during either exercise protocol, which were of a remarkably similar magnitude to rest. In contrast, FENT administration reduced the exercise-induced resetting of the operating point for MAP and HR during both EVO (116 ± 10 mmHg to 100 ± 15 mmHg and 93 ± 14 bpm to 82 ± 10 bpm) and VOL (107 ± 13 mmHg to 100 ± 17 mmHg and 89 ± 10 bpm to 72 ± 10 bpm) exercise bouts. Together, these findings document that group III/IV muscle afferent feedback is critical for the resetting of the carotid baroreflex MAP and HR operating points, independent of exercise-induced changes in central command, but not for spontaneous carotid baroreflex responsiveness.

Keywords: carotid baroreflex; central command; exercise pressor reflex; metaboreflex.

Figure 1. Mean arterial pressure (MAP) and heart rate (HR) responses to electrically evoked and voluntary quadriceps contractions

Each data point represents the average over the preceding minute. Data are presented as mean ± SD.

Figure 2. Carotid baroreflex control of mean arterial pressure (MAP) and heart rate (HR) during electrically evoked quadriceps contractions

A and C, carotid baroreflex‐mediated response to neck pressure (NP) and neck suction (NS) for MAP (A) and HR (C) at rest and during exercise under control conditions (CTRL) and following lumbar intrathecal fentanyl (FENT) injection. For each condition, the three data points represent (from left to right) the response to NP (+40 mmHg), the operating point and the response to NS (−60 mmHg). B and D, quantification of the carotid baroreflex‐mediated response to NP and NS for MAP (B) and HR (D) expressed as a change from the operating point. Data are presented as mean ± SD. ^* P < 0.05 vs. Rest. †P < 0.05 vs. FENT.

Figure 3. Carotid baroreflex control of mean arterial pressure (MAP) and heart rate (HR) during voluntary quadriceps contractions

A and C, carotid baroreflex‐mediated response to neck pressure (NP) and neck suction (NS) for MAP (A) and HR (C) at rest and during exercise under control conditions (CTRL) and following lumbar intrathecal fentanyl (FENT) injection. For each condition, the three data points represent (from left to right) the response to NP (+40 mmHg), the operating point, and the response to NS (−60 mmHg). B and D, quantification of the carotid baroreflex‐mediated response to NP and NS for MAP (B) and HR (D) are expressed as a change from the operating point. Data are presented as mean ± SD. ^* P < 0.05 vs. Rest. †P < 0.05 vs. FENT.

Figure 4. Effect of fentanyl on the pressor response to electrically evoked quadriceps contractions

Calculations were performed on MAP at the operating point between the 4th and the 10th minute (i.e. ‘steady state’). Data are presented as mean ± SD. ^* P < 0.05 vs. CTRL.