Time for Radical Changes in Brain Stem Nomenclature—Applying the Lessons From Developmental Gene Patterns

Watson, Charles; Bartholomaeus, Caitlin; Puelles, Luis

doi:10.3389/fnana.2019.00010

Cited by 61 publications

(75 citation statements)

References 62 publications

(102 reference statements)

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“…The midbrain ROI has special implications for pain, negative emotion and neurobehavioural dysfunction in ME/CFS and GWI. Recent studies of brain development and prosomeric genoarchitectonics have led to new perspectives into the origins and nomenclature of midbrain and hindbrain structures that have been embraced by the 2017 Terminological Neuroanatomica of the Federative International Programme for Anatomical Terminology (Anatomists; Puelles, 2016 , 2019 ; Watson et al , 2019 ). The diencephalon forms in response to dorsal–ventral gradients of Pax6 and Otx2.…”

Section: Discussionmentioning

confidence: 99%

Exercise alters brain activation in Gulf War Illness and Myalgic Encephalomyelitis/Chronic Fatigue Syndrome

Washington

Rayhan

Garner

et al. 2020

Brain Communications

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Gulf War Illness affects 25–30% of American veterans deployed to the 1990–91 Persian Gulf War and is characterized by cognitive post-exertional malaise following physical effort. Gulf War Illness remains controversial since cognitive post-exertional malaise is also present in the more common Myalgic Encephalomyelitis/Chronic Fatigue Syndrome. An objective dissociation between neural substrates for cognitive post-exertional malaise in Gulf War Illness and Myalgic Encephalomyelitis/Chronic Fatigue Syndrome would represent a biological basis for diagnostically distinguishing these two illnesses. Here, we used functional magnetic resonance imaging to measure neural activity in healthy controls and patients with Gulf War Illness and Myalgic Encephalomyelitis/Chronic Fatigue Syndrome during an N-back working memory task both before and after exercise. Whole brain activation during working memory (2-Back > 0-Back) was equal between groups prior to exercise. Exercise had no effect on neural activity in healthy controls yet caused deactivation within dorsal midbrain and cerebellar vermis in Gulf War Illness relative to Myalgic Encephalomyelitis/Chronic Fatigue Syndrome patients. Further, exercise caused increased activation among Myalgic Encephalomyelitis/Chronic Fatigue Syndrome patients within the dorsal midbrain, left operculo-insular cortex (Rolandic operculum) and right middle insula. These regions-of-interest underlie threat assessment, pain, interoception, negative emotion and vigilant attention. As they only emerge post-exercise, these regional differences likely represent neural substrates of cognitive post-exertional malaise useful for developing distinct diagnostic criteria for Gulf War Illness and Myalgic Encephalomyelitis/Chronic Fatigue Syndrome.

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Section: Discussionmentioning

confidence: 99%

Exercise alters brain activation in Gulf War Illness and Myalgic Encephalomyelitis/Chronic Fatigue Syndrome

Washington

Rayhan

Garner

et al. 2020

Brain Communications

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“…The current manuscript provides a comprehensive description of the organization of the brainstem (midbrain, pons, and medulla oblongata) and cerebellum of the tree pangolin (encompassing the region of the brain developmentally defined as diencephalic prosomere 1 through to rhombomere 11, Watson et al, ). As indicated by earlier studies (Bautista & Foltz, ; Chang, ; Cooper et al, ; Elliot Smith, ; Lee et al, ; Weber, ), broadly speaking, the brainstem and cerebellum evince an organization that would be considered typical for mammals (Manger, ).…”

Section: Discussionmentioning

confidence: 99%

“…The nomenclature used in the current study was taken from Paxinos, Watson, Carrive, Kirkcaldie, and Ashwell (), but when variances occurred, other nomenclature was applied. In addition, the proposed new nomenclature for these regions of the brain (Watson et al, ) is given where relevant. Digital photomicrographs were captured using a Zeiss Axioskop and Zen software.…”

Section: Methodsmentioning

confidence: 99%

“…The brainstem and cerebellum are readily identifiable structures within the caudal aspect of the mammalian brain. The brainstem, as defined here, is composed of three distinct regions, the midbrain, pons, and medulla oblongata (Manger, ), although, based on developmental patterns of gene expression, a major change in the way we define, parcellate and describe the brainstem and adjacent regions has been proposed (e.g., Watson, Bartholomaeus, & Puelles, ). In this sense, we herein describe the brain of the tree pangolin from the level of diencephalic prosomere 1 through to rhombomere 11.…”

Section: Introductionmentioning

confidence: 99%

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The brain of the tree pangolin (Manis tricuspis). VI. The brainstem and cerebellum

Imam

Bhagwandin

Ajao

et al. 2019

J of Comparative Neurology

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The brainstem (midbrain, pons, and medulla oblongata) and cerebellum (diencephalic prosomere 1 through to rhombomere 11) play central roles in the processing of sensorimotor information, autonomic activity, levels of awareness and the control of functions external to the conscious cognitive world of mammals. As such, comparative analyses of these structures, especially the understanding of specializations or reductions of structures with functions that have been elucidated in commonly studied mammalian species, can provide crucial information for our understanding of the behavior of less commonly studied species, like pangolins. In the broadest sense, the nuclear complexes and subdivisions of nuclear complexes, the topographical arrangement, the neuronal chemistry, and fiber pathways of the tree pangolin conform to that typically observed across more commonly studied mammalian species. Despite this, variations in regions associated with the locus coeruleus complex, auditory system, and motor, neuromodulatory and autonomic systems involved in feeding, were observed in the current study. While we have previously detailed the unusual locus coeruleus complex of the tree pangolin, the superior olivary nuclear complex of the auditory system, while not exhibiting additional nuclei or having an altered organization, this nuclear complex, particularly the lateral superior olivary nucleus and nucleus of the trapezoid body, shows architectonic refinement. The cephalic decussation of the pyramidal tract, an enlarged hypoglossal nucleus, an additional subdivision of the serotonergic raphe obscurus nucleus, and the expansion of the superior salivatory nucleus, all indicate neuronal specializations related to the myrmecophagous diet of the pangolins.

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“…A similar antero-inferior cerebellar artery with identical neuromeric topography exists in the mouse, which serves a large part of the IVth ventricle chorioidal plexus and then jumps into the caudal cerebellum (r1; Scremin and Holschneider, 2012). The lateral short and long circumferential pontine arteries are also ventral and dorsal alar branches of the basilar artery at pontine levels, corresponding at least to r3 and r4 (va, da; Figures 1D, 8B), but possibly also to r2 and r1 (since the pontine formation partly covers these domains as well; see Watson et al, 2019, this book). We did not find useful human data specifically on r2 and r1 vascularization (apparently, these domains were not recognized as distinct regions in conventional columnar neuroanatomy), but we expect that these neuromeric units (important because they hold most of the principal sensory and motor trigeminal nuclei, apart of vestibulocochlear centers; Puelles, 2013) are also served in their alar domains by segment-specific lateral (ventral and dorsal alar) circumferential prepontine arteries that probably have been observed, but were misclassified as “pontine” (va, da; Figure 8B).…”

Section: Resultsmentioning

confidence: 91%

Patterned Vascularization of Embryonic Mouse Forebrain, and Neuromeric Topology of Major Human Subarachnoidal Arterial Branches: A Prosomeric Mapping

et al. 2019

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The prosomeric brain model contemplates progressive regionalization of the central nervous system (CNS) from a molecular and morphological ontogenetic perspective. It defines the forebrain axis relative to the notochord, and contemplates intersecting longitudinal (zonal, columnar) and transversal (neuromeric) patterning mechanisms. A checkboard pattern of histogenetic units of the neural wall results, where each unit is differentially fated by an unique profile of active genes. These natural neural units later expand their radial dimension during neurogenesis, histogenesis, and correlative differential morphogenesis. This fundamental topologic framework is shared by all vertebrates, as a Bauplan, each lineage varying in some subtle aspects. So far the prosomeric model has been applied only to neural structures, but we attempt here a prosomeric analysis of the hypothesis that major vessels invade the brain wall in patterns that are congruent with its intrinsic natural developmental units, as postulated in the prosomeric model. Anatomic and embryologic studies of brain blood vessels have classically recorded a conserved pattern of branches (thus the conventional terminology), and clinical experience has discovered a standard topography of many brain arterial terminal fields. Such results were described under assumptions of the columnar model of the forebrain, prevalent during the last century, but this is found insufficient in depth and explanatory power in the modern molecular scenario. We have thus explored the possibility that brain vascularization in rodents and humans may relate systematically to genoarchitectonic forebrain subdivisions contemplated in the prosomeric model. Specifically, we examined first whether early vascular invasion of some molecularly characterized prosomeric domains shows heterochrony. We indeed found a heterochronic pattern of vascular invasion that distinguishes between adjacent brain areas with differential molecular profiles. We next mapped topologically on the prosomeric model the major arterial branches serving the human brain. The results of this approach bear on the possibility of a developmentally-based modern arterial terminology.

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Time for Radical Changes in Brain Stem Nomenclature—Applying the Lessons From Developmental Gene Patterns

Cited by 61 publications

References 62 publications

Exercise alters brain activation in Gulf War Illness and Myalgic Encephalomyelitis/Chronic Fatigue Syndrome

Exercise alters brain activation in Gulf War Illness and Myalgic Encephalomyelitis/Chronic Fatigue Syndrome

The brain of the tree pangolin (Manis tricuspis). VI. The brainstem and cerebellum

Patterned Vascularization of Embryonic Mouse Forebrain, and Neuromeric Topology of Major Human Subarachnoidal Arterial Branches: A Prosomeric Mapping

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