Electrophysiological analysis of midbrain periaqueductal gray influence on cardiovascular neurons in the ventrolateral medulla oblongata

Plas, van der Johannes; Maes, F.W.; Bohus, B.

doi:10.1016/0361-9230(95)02012-g

Cited by 22 publications

(18 citation statements)

References 41 publications

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“…Indeed, electrical stimulation can still be used to specifically activate different components with specific stimulating parameters (3,25). As previously suggested (14), lowintensity and high-frequency electrical stimulations elicited similar cardiovascular and respiratory responses from the dPAG as chemical disinhibition.…”

Section: Discussionmentioning

confidence: 81%

“…Electrical dPAG stimulation is the technique of choice since the on-and off-stimulation timing can be reliably determined. Although electrical stimulation activates both neurons and fibers of passage, it has been demonstrated that controlled electrical stimulation in the dPAG elicits cardiorespiratory responses similar to chemical stimulation (3,14,25). Intensity-or frequency-dependent physiological responses have been described with electrical stimulation in the PAG (24,28).…”

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confidence: 97%

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Respiratory muscle responses elicited by dorsal periaqueductal gray stimulation in rats

Zhang¹,

Hayward²,

Davenport³

2005

American Journal of Physiology-Regulatory, Integrative and Comp

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The periaqueductal gray matter is an essential neural substrate for central integration of defense behavior and accompanied autonomic responses. The dorsal half of the periaqueductal gray matter (dPAG) is also involved in mediating emotional responses of anxiety and fear, psychological states that often are associated with changes in ventilation. However, information regarding respiratory modulation elicited from this structure is limited. The present study was undertaken to investigate the relationship between stimulus frequency and magnitude on ventilatory pattern and respiratory muscle activity in urethane-anesthetized, spontaneously breathing rats. Electrical stimulation in the dPAG-recruited abdominal muscle activity increased ventilation and increased respiratory frequency by significantly shortening both inspiratory time and expiratory time. Ventilation increased within the first breath after the onset of stimulation, and the respiratory response increased with increasing stimulus frequency and magnitude. dPAG stimulation also increased baseline EMG activity in the diaphragm and recruited baseline external abdominal oblique EMG activity, normally quiescent during eupneic breathing. Significant changes in cardiorespiratory function were only evoked by stimulus intensities >10 microA and when stimulus frequencies were >10 Hz. Respiratory activity of both the diaphragm and abdominal muscles remained elevated for a minimum of 60 s after cessation of stimulation. These results demonstrate that there is a short-latency respiratory response elicited from the dPAG stimulation, which includes both inspiratory and expiratory muscles. The changes in respiratory timing suggest rapid onset and sustained poststimulus dPAG modulation of the brain stem respiratory network that includes expiratory muscle recruitment.

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Section: Discussionmentioning

confidence: 81%

mentioning

confidence: 97%

Respiratory muscle responses elicited by dorsal periaqueductal gray stimulation in rats

Zhang¹,

Hayward²,

Davenport³

2005

American Journal of Physiology-Regulatory, Integrative and Comp

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“…The observation of both asymmetric and symmetric synapses formed by PAG axons indicates that this pathway arises from phenotypically diverse populations of cells. Electrophysiological analyses of VTA responses to PAG stimulation have not yet been conducted, but in other target areas, stimulation evokes mixed excitation and inhibition (Lovick 1992; Snowball et al 1997; van der Plas et al 1995). Given the functional distinction between dorsal and ventral divisions of the PAG (Lovick 1992) (see below), synaptic morphology might reflect the region of origin within the PAG, but this was not observed in the present study.…”

Section: Discussionmentioning

confidence: 99%

Periaqueductal gray afferents synapse onto dopamine and GABA neurons in the rat ventral tegmental area

Omelchenko

Sesack

2009

J of Neuroscience Research

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The midbrain central gray (periaqueductal gray; PAG) mediates defensive behaviors and is implicated in the rewarding effects of opiate drugs. Projections from the PAG to the ventral tegmental area (VTA) suggest that this region might also regulate behaviors involving motivation and cognition. However, studies have not yet examined the morphological features of PAG axons in the VTA or whether they synapse onto dopamine (DA) or GABA neurons. In this study, we injected anterograde tracers into the rat PAG and used immunoperoxidase to visualize the projections to the VTA. Immunogold-silver labeling for tyrosine hydroxylase (TH) or GABA was then used to identify the phenotype of innervated cells. Electron microscopic examination of the VTA revealed axons labeled anterogradely from the PAG, including myelinated and unmyelinated fibers and axon varicosities, some of which formed identifiable synapses. Approximately 55% of these synaptic contacts were of the symmetric (presumably inhibitory) type; the rest were asymmetric (presumably excitatory). These findings are consistent with the presence of both GABA and glutamate projection neurons in the PAG. Some PAG axons contained dense-cored vesicles indicating the presence of neuropeptides in addition to classical neurotransmitters. PAG projections synapsed onto both DA and GABA cells with no obvious selectivity, providing the first anatomical evidence for these direct connections. The results suggest a diverse nature of PAG physiological actions on midbrain neurons. Moreover, as both the VTA and PAG are implicated in the reinforcing actions of opiates, our findings provide a potential substrate for some of the rewarding effects of these drugs.

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“…We observed differential activity in dorsal pons, right insula and somatosensory cortex associated with a pathological condition that leads (because of the peripheral autonomic denervation in PAF) to an uncoupling of central efferent control and afferent feedback of autonomic responses. In the pons, task-independent differential activity was present in a dorsal region that encompassed nuclei involved in control and representation of autonomic responses 21 , in particular, the parabrachial nucleus 22,23 and periaqueductal gray 24 . Group differences in dorsal pons activity, commonly expressed across task, are consistent with a proposal that the pons has homeostatic involvement in autonomic regulation, and does not provide context-specific representation of peripheral arousal.…”

Section: Discussionmentioning

confidence: 99%

Neuroanatomical basis for first- and second-order representations of bodily states

2001

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articles Emotional, cognitive and physical behaviors mediated by the central nervous system are integrated with peripheral changes in bodily states. Moreover, physiological changes in bodily state directly influence emotional expression 1,2 and cognitive functions such as decision-making 3 and memory 4 . At a broader level, emotions may be subsumed within homeostatic mechanisms that underlie survival of the organism 2,5 . In a theoretical model 5 based on neurological observations, prime emphasis is given to the cerebral representation of bodily states as a substrate for emotions and conscious awareness. Fundamental components of the model are first-order autoregulatory mappings and second-order re-mappings of bodily states consequent upon behavioral experience. The dorsal pons is proposed to support first-order mapping of bodily state, because of its involvement in homeostatic regulation mediated via afferent information from the body. The model also proposes that somatosensory areas, the somatosensory cortices and insula, contribute to this primary representation of bodily states. In contrast, cingulate and medial parietal cortices are critical components in second-order mappings of experience-dependent changes in body states.Here we tested specific predictions arising from these theoretical considerations. We compared the state-dependent regional brain activity in healthy human subjects with activity in subjects with pure autonomic failure (PAF) 6 . PAF is an idiopathic disorder acquired in middle age that only affects the peripheral autonomic nervous system. Subjects with PAF cannot modulate their bodily state via the autonomic nervous system because of peripheral autonomic denervation, but have no other neurological deficit (sensory or motor). Consequently, there is no integrated central feedback of information concerning autonomic changes that are normal accompaniments of ongoing behavior 6 . Peripheral autonomic denervation results in a failure of neurogenic control of circulation, the cardinal feature of which is orthostatic (postural) hypotension due to an inability to activate sympathetic pathways to engender vasoconstriction during gravitational challenges [6][7][8] . Additionally, subjects with PAF do not generate heart rate and blood pressure increases during effortful exercise or mental arithmetic (stressor tasks) 6 and do not increase circulating catecholamines during physical or emotional challenge 6 . These subjects have absent sympathetic skin conductance responses to emotive and orienting stimuli 9 , and have diminished pupilliary reflexes 10 . Through histological evidence, PAF has been associated with Lewy bodies in peripheral autonomic ganglia 11 , but its cause is unknown 6 . PAF is distinguished from central neurodegenerative causes of autonomic failure (such as multiple system atrophy or Parkinson's disease with autonomic failure) by normal life expectancy 6,7 , and by the absence of clinical and hormonal 12 indicators of central neurological degeneration. Similarly, gross and pervasive...

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Electrophysiological analysis of midbrain periaqueductal gray influence on cardiovascular neurons in the ventrolateral medulla oblongata

Cited by 22 publications

References 41 publications

Respiratory muscle responses elicited by dorsal periaqueductal gray stimulation in rats

Respiratory muscle responses elicited by dorsal periaqueductal gray stimulation in rats

Periaqueductal gray afferents synapse onto dopamine and GABA neurons in the rat ventral tegmental area

Neuroanatomical basis for first- and second-order representations of bodily states

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