Amygdala mediates respiratory responses to sudden arousing stimuli and to restraint stress in rats

Abstract

Bondarenko E, Hodgson DM, Nalivaiko E. Amygdala mediates respiratory responses to sudden arousing stimuli and to restraint stress in rats. Am J Physiol Regul Integr Comp Physiol 306: R951-R959, 2014. First published April 16, 2014 doi:10.1152/ajpregu.00528.2013.-Both human and animal studies have demonstrated that respiratory parameters change in response to presentation of alerting stimuli, as well as during stress, yet central neuronal pathways that mediate such responses remain unknown. The aim of our study was to investigate the involvement of the amygdala in mediating respiratory responses to stressors of various intensities and duration. Adult male Wistar rats (n ϭ 8) received microinjections of GABAA agonist muscimol or saline into the amygdala bilaterally and were subjected to a respiratory recording using whole body plethysmography. Presentation of acoustic stimuli (500-ms white noise, 40 -90 dB) caused transient responses in respiratory rate that were proportional to the stimulus intensity, ranging from ϩ13 Ϯ 9 cpm to ϩ276 Ϯ 67 cpm for 40-and 90-dB stimuli, respectively. Inhibition of the amygdala significantly suppressed respiratory rate responses to the high-intensity stimuli (70 -90 dB). Submitting rats to the restraint stress significantly elevated the mean respiratory rate (ϩ72 Ϯ 8 cpm) and the dominant respiratory rate (ϩ51 Ϯ 12 cpm), as well as the fraction of high-frequency respiratory rate (ϩ10 Ϯ 3%). Inhibition of the amygdala by muscimol significantly suppressed these responses. We conclude that the amygdala is one of the key structures that are essential for expression of respiratory responses to stressful or alerting stimuli in rats.

Central mechanisms regulating coordinated cardiovascular and respiratory function during stress and arousal

“…In animals, brief alerting stimuli such as an unexpected noise or light will evoke immediate autonomic and respiratory responses, characterized by strong cutaneous vasoconstriction and respiratory activation (17,18,84,109,161). In contrast, such nonnoxious brief stimuli evoke only small and transient increases in arterial pressure and little or no changes in blood flow to the mesenteric, renal, and hindlimb vascular beds (109,162), indicating that the sympathetic outflow to the cutaneous vascular bed is rather selectively activated by mild alerting stimuli.…”

“…Later, Blanchard and Blanchard (15) showed that this was due specifically to lesions of the amygdaloid complex. More recently, it has been shown that inhibition of neurons in the amygdaloid nuclei by microinjection of muscimol greatly reduces both the cutaneous vasoconstrictor and respiratory responses evoked by brief alerting stimuli such as noise or light (18,109,162). Furthermore, lesions of the amygdaloid complex also reduce the hindlimb vasodilation and mesenteric vasoconstriction that are evoked by a more prolonged threatening stimulus (65).…”

Prelimbic prefrontal cortex mediates respiratory responses to mild and potent prolonged, but not brief, stressors

“…Resp Rate DOMINANT was assessed as a mode of each of these histograms, while %HF was assessed as the ratio AUC 250-650 /AUC 0-650 (AUC = area under the curve). See Bondarenko et al (2014) and Carnevali et al (2013) for more detailed descriptions of this procedure.…”

“…Inhibition of the amygdala or of the dorsomedial hypothalamus produces decreases in stress-induced tachycardic, pressor and tachypnoeic responses (Bondarenko et al, 2013(Bondarenko et al, , 2014McDougall et al, 2004). Conversely, activation of these areas produces increases in heart and respiratory rates as well as an increase in arterial pressure (Applegate et al, 1983;McDowall et al, 2007).…”

Limbic modulation of the autonomic nervous system

“…Inactivation and lesion-based studies have identified the hippocampus and amygdala as perhaps the most pivotal structures, particularly in relation to fear, anxiety and stress responses (Bannerman et al, 2003;Pentkowski et al, 2006;Bondarenko et al, 2014;Felix-Ortiz and Tye, 2014;Zhang et al, 2014;Sandi and Haller, 2015). However, knowledge of the contributions of each region in generating specific physiological responses remains limited.…”