Disinhibition of the midbrain colliculi unmasks coordinated autonomic, respiratory, and somatomotor responses to auditory and visual stimuli

Abstract

The midbrain superior and inferior colliculi have critical roles in generating coordinated orienting or defensive behavioral responses to environmental stimuli, and it has been proposed that neurons within the colliculi can also generate appropriate cardiovascular and respiratory responses to support such behavioral responses. We have previously shown that activation of neurons within a circumscribed region in the deep layers of the superior colliculus and in the central and external nuclei of the inferior colliculus can evoke a response characterized by intense and highly synchronized bursts of renal sympathetic nerve activity and phrenic nerve activity. In this study, we tested the hypothesis that, under conditions in which collicular neurons are disinhibited, coordinated cardiovascular, somatomotor, and respiratory responses can be evoked by natural environmental stimuli. In response to natural auditory, visual, or somatosensory stimuli, powerful synchronized increases in sympathetic, respiratory, and somatomotor activity were generated following blockade of GABAA receptors in a specific region in the midbrain colliculi of anesthetized rats, but not under control conditions. Such responses still occurred after removal of most of the forebrain, including the amygdala and hypothalamus, indicating that the essential pathways mediating these coordinated responses were located within the brain stem. The temporal relationships between the different outputs suggest that they are driven by a common population of "command neurons" within the colliculi.

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

“…6). Although the evoked responses were highly synchronized, the onsets of the evoked increases in respiratory and somatomotor activity slightly preceded the onset of the evoked increases in sympathetic activity (114) (Fig. 6, B and C).…”

“…In contrast, as illustrated in Fig. 6C, in response to auditory, visual, or somatosensory stimulation following disinhibition of certain sites in the colliculi, the increase in spSNA occurs primarily during the inspiratory phase of respiration (i.e., when phrenic nerve activity is increased) (114). It therefore seems unlikely that the observed sympathetic-respiratory synchronization is simply a consequence of sympathetic premotor neurons receiving a modulatory input from central respiratory neurons that in turn are activated by inputs from the colliculi.…”

“…Similarly, the inferior colliculus (IC), which receives convergent signals from brain stem auditory nuclei, can also generate appropriate behavioral responses to auditory signals via projections to the SC (30). In a recent study in anesthetized rats, my colleagues and I (114) found that natural auditory, visual, and somatosensory stimuli could evoke highly synchronized increases in sympathetic, respiratory, and somatomotor activity, but only after disinhibition (by microinjection of the GABA receptor antagonists picrotoxin or bicuculline) of certain sites within the SC or IC (Fig. 6).…”

“…At the same time, there are significant differences in the connections of the dlPAG and deep layers of SC; for example, there is a dense projection from the medial prefrontal cortex to the dlPAG but not to the adjacent SC (4) and a descending projection to the pontomedullary reticular formation from the deep layers of SC but not from the dlPAG (42,128). Furthermore, cardiovascular and respiratory responses evoked from the dlPAG, but not those evoked from the SC, are dependent on the activation of the DMH (48,77,114). Thus, although the dlPAG and deep layers of the SC have some features in common, they appear to be essentially distinct defense systems.…”

Afferent and efferent connections of C1 cells with spinal cord or hypothalamic projections in mice

“…The respiratory modulation of the C1 neurons could also originate from respiratory-related neurons in the reticular core (Haselton and Guyenet 1989a, b). The first order neurons in the superficial and deep layers of inferior and superior colliculus may mediate the autonomic response to sudden visual or acoustic stimuli (Muller-Ribeiro et al 2014). Stimulation of sites in ventrolateral PAG in the same area where we report first order projecting neurons can modulate responses in RVLM neurons (Lovick 1992a, b).…”