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Reassessment of the structural basis of the ascending arousal system
Abstract
The “ascending reticular activating system” theory proposed that neurons in the upper brainstem reticular formation projected to forebrain targets that promoted wakefulness. More recent formulations have emphasized that most neurons at the pontomesencephalic junction that participate in these pathways are actually in monoaminergic and cholinergic cell groups. However, cell‐specific lesions of these cell groups have never been able to reproduce the deep coma seen after acute paramedian midbrain lesions that transect ascending axons at the caudal midbrain level. To determine whether the cortical afferents from the thalamus or the basal forebrain were more important in maintaining arousal, we first placed large cell‐body‐specific lesions in these targets. Surprisingly, extensive thalamic lesions had little effect on electroencephalographic (EEG) or behavioral measures of wakefulness or on c‐Fos expression by cortical neurons during wakefulness. In contrast, animals with large basal forebrain lesions were behaviorally unresponsive and had a monotonous sub‐1‐Hz EEG, and little cortical c‐Fos expression during continuous gentle handling. We then retrogradely labeled inputs to the basal forebrain from the upper brainstem, and found a substantial input from glutamatergic neurons in the parabrachial nucleus and adjacent precoeruleus area. Cell‐specific lesions of the parabrachial‐precoeruleus complex produced behavioral unresponsiveness, a monotonous sub‐1‐Hz cortical EEG, and loss of cortical c‐Fos expression during gentle handling. These experiments indicate that in rats the reticulo‐thalamo‐cortical pathway may play a very limited role in behavioral or electrocortical arousal, whereas the projection from the parabrachial nucleus and precoeruleus region, relayed by the basal forebrain to the cerebral cortex, may be critical for this process. J. Comp. Neurol. 519:933–956, 2011. © 2010 Wiley‐Liss, Inc.
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In the citing paper
“Evidence that the AAn is essential for consciousness comes from experimentally induced lesions in rodents3 and cats4 and mapping of brainstem infarctions in humans.5”
From Disruption of the ascending arousal network in acute traumatic disorders of consciousness (2019) · cites this paper as [3]
In the citing paper
“In addition, several brainstem nuclei (locus coeruleus, dorsal raphe, median raphe, pedunculopontine nucleus, parabrachial nucleus), non-specific thalamic nuclei, hypothalamus, and basal forebrain are also included in the ARAS system (Aston-Jones et al., 2001; Parvizi and Damasio, 2003; Fuller et al., 2011).”
From The Ascending Reticular Activating System from Pontine Reticular Formation to the Thalamus in the Human Brain (2013) · cites this paper as Fuller et al., 2011
In the citing paper
“Similarly, our findings are consistent with previous work linking dorsolateral pontine tegmentum lesions to coma in humans1,4 and coma-like outcomes in animals.9”
From Thalamic strokes that severely impair arousal extend into the brainstem (2018) · cites this paper as [9]
In the citing paper
“These results are consistent with growing evidence that pathways most critical for human arousal lie outside the thalamus.”
From Thalamic strokes that severely impair arousal extend into the brainstem (2018) · cites this paper as [9]
In the citing paper
“Yet the assumption that critical, arousal-promoting projections from the brainstem must synapse in the thalamus has been challenged by a growing body of research in experimental animals.”
From Thalamic strokes that severely impair arousal extend into the brainstem (2018) · cites this paper as [9]
In the citing paper
“Ablating the posterior hypothalamus or inhibiting corticopetal neurons in the basal forebrain nuclei produces coma, whereas exciting these regions is potently wake-promoting.3,9,11–13”
From Thalamic strokes that severely impair arousal extend into the brainstem (2018) · cites this paper as [9]
In the citing paper
“Ablating the posterior hypothalamus or inhibiting corticopetal neurons in the basal forebrain nuclei produces coma, whereas exciting these regions is potently wake-promoting.3,9,11–13”
From Thalamic strokes that severely impair arousal extend into the brainstem (2018) · cites this paper as [9]
In the citing paper
“For example, extensive ablation or inhibition of thalamic neurons fails to alter the normal pattern and amount of waking and sleeping behavior, and the only apparent electroencephalographic abnormality that results is a loss of spindle activity during sleep.8–10”
From Thalamic strokes that severely impair arousal extend into the brainstem (2018) · cites this paper as [9]
In the citing paper
“Outside the thalamus, neurons in the posterior hypothalamus and basal forebrain appear more important than the thalamus for linking brainstem arousal- promoting projections to the cerebral cortex.”
From Thalamic strokes that severely impair arousal extend into the brainstem (2018) · cites this paper as [9]
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Metadata
- Authors
- Fuller, P., Sherman, D., Pedersen, N. P., Saper, C. B., & Lu, J.
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2011-01-28
- Volume
- 519
- Issue
- 5
- Pages
- 933-956
- ISSN
- 0021-9967
- 1096-9861
- PMC
- PMC3119596
- Cited by
- 465
- References
- 4
- Language
- en
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