Partial loss in septo-hippocampal cholinergic neurons alters memory-dependent measures of brain connectivity without overt memory deficits

Brayda-Bruno, Laurent; Mons, Nicole; Yee, Benjamin K.; Micheau, Jacques; Abrous, Djoher Nora; Nogués, Xavier; Marighetto, Aline

doi:10.1016/j.nbd.2013.01.010

Cited by 10 publications

(6 citation statements)

References 55 publications

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“…As a first step toward such applications, we demonstrated that the dissociated FC profiles of the identified CBF subdivisions are reproducible in rs‐fMRI acquisitions of elderly participants as typically collected in clinical research settings. We expect rs‐fMRI‐based assessments of CBF connectivity to be particularly useful for the study of functional CBF alterations in predementia stages of neurodegenerative disease (Brayda‐Bruno et al, ; Grothe, Ewers, Krause, Heinsen, & Teipel, ; Lim et al, ; Ray et al, ), as well as other neuropsychiatric conditions with cholinergic involvement that are not typically associated with gross neurodegeneration (Grothe et al, ; Perry et al, ; Sarter et al, ).…”

Section: Resultsmentioning

confidence: 99%

“…We expect rs-fMRI-based assessments of CBF connectivity to be particularly useful for the study of functional CBF alterations in predementia stages of neurodegenerative disease (Brayda-Bruno et al, 2013;Grothe, Ewers, Krause, Heinsen, & Teipel, 2014;Lim et al, 2015;Ray et al, 2017), as well as other neuropsychiatric conditions with cholinergic involvement that are not typically associated with gross neurodegeneration Perry et al, 2001;Sarter et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

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The corticotopic organization of the human basal forebrain as revealed by regionally selective functional connectivity profiles

Fritz

Ray

Dyrba

et al. 2018

Human Brain Mapping

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The cholinergic basal forebrain (CBF), comprising different groups of cortically projecting cholinergic neurons, plays a crucial role in higher cognitive processes and has been implicated in diverse neuropsychiatric disorders. A distinct corticotopic organization of CBF projections has been revealed in animal studies, but little is known about their organization in the human brain. We explored regional differences in functional connectivity (FC) profiles within the human CBF by applying a clustering approach to resting‐state functional magnetic resonance imaging (rs‐fMRI) data of healthy adult individuals (N = 85; 19–85 years). We further examined effects of age on FC of the identified CBF clusters and assessed the reproducibility of cluster‐specific FC profiles in independent data from healthy older individuals (N = 25; 65–89 years). Results showed that the human CBF is functionally organized into distinct anterior‐medial and posterior‐lateral subdivisions that largely follow anatomically defined boundaries of the medial septum/diagonal band and nucleus basalis Meynert. The anterior‐medial CBF subdivision was characterized by connectivity with the hippocampus and interconnected nodes of an extended medial cortical memory network, whereas the posterior‐lateral subdivision was specifically connected to anterior insula and dorsal anterior cingulate components of a salience/attention network. FC of both CBF subdivisions declined with increasing age, but the overall topography of subregion‐specific FC profiles was reproduced in independent rs‐fMRI data of healthy older individuals acquired in a typical clinical setting. Rs‐fMRI‐based assessments of subregion‐specific CBF function may complement established volumetric approaches for the in vivo study of CBF involvement in neuropsychiatric disorders.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

The corticotopic organization of the human basal forebrain as revealed by regionally selective functional connectivity profiles

Fritz

Ray

Dyrba

et al. 2018

Human Brain Mapping

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“…These are severely involved in AD (Davies and Maloney, 1976 ; Coyle et al, 1983 ; Sassin et al, 2000 ). In particular, degeneration of Ch1 and Ch2 neurons is responsible for the loss of septo-hippocampal connections leading to memory impairment (Gertz et al, 1987 ; Brayda-Bruno et al, 2013 ). The Ch4 (nucleus basalis of Meynert) nuclear complex, which is divided into various subfields (Mesulam, 2013 ) and receives dense NE projections from LC degenerates as well (Mesulam et al, 1983a , b , 1984 ; Mesulam and Geula, 1988 ; Smiley and Mesulam, 1999 ; Haghdoost-Yazdi et al, 2009 ).…”

Section: The Neuroanatomy Of Lc In Admentioning

confidence: 99%

The Neuroanatomy of the Reticular Nucleus Locus Coeruleus in Alzheimer’s Disease

et al. 2017

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Alzheimer’s Disease (AD) features the accumulation of β-amyloid and Tau aggregates, which deposit as extracellular plaques and intracellular neurofibrillary tangles (NFTs), respectively. Neuronal Tau aggregates may appear early in life, in the absence of clinical symptoms. This occurs in the brainstem reticular formation and mostly within Locus Coeruleus (LC), which is consistently affected during AD. LC is the main source of forebrain norepinephrine (NE) and it modulates a variety of functions including sleep-waking cycle, alertness, synaptic plasticity, and memory. The iso-dendritic nature of LC neurons allows their axons to spread NE throughout the whole forebrain. Likewise, a prion-like hypothesis suggests that Tau aggregates may travel along LC axons to reach out cortical neurons. Despite this timing is compatible with cross-sectional studies, there is no actual evidence for a causal relationship between these events. In the present mini-review, we dedicate special emphasis to those various mechanisms that may link degeneration of LC neurons to the onset of AD pathology. This includes the hypothesis that a damage to LC neurons contributes to the onset of dementia due to a loss of neuroprotective effects or, even the chance that, LC degenerates independently from cortical pathology. At the same time, since LC neurons are lost in a variety of neuropsychiatric disorders we considered which molecular mechanism may render these brainstem neurons so vulnerable.

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“…Furthermore, a significant correlation between cognitive impairment and decline in cholinergic markers for the septo-hippocampal projection in aged rats (Gallagher et al, 1990 ; Smith and Booze, 1995 ) supports the involvement of BF cholinergic neurons in cognition. More recently, animals with a saporin-induced partial loss of septo-hippocampal cholinergic neurons exhibited cognitive deficit (Brayda-Bruno et al, 2013 ). Other lesion studies extended the importance of the BF cholinergic system in the process of functional recovery from brain injury in young rats (Conner et al, 2005 ), which is intriguing in that animals with BF lesions may show deficits in cognitive function.…”

Section: Overview Of the Basal Forebrain Cholinergic Systemmentioning

confidence: 99%

Interaction of basal forebrain cholinergic neurons with the glucocorticoid system in stress regulation and cognitive impairment

Paul

Jeon

Bizon

et al. 2015

Front. Aging Neurosci.

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A substantial number of studies on basal forebrain (BF) cholinergic neurons (BFCN) have provided compelling evidence for their role in the etiology of stress, cognitive aging, Alzheimer’s disease (AD), and other neurodegenerative diseases. BFCN project to a broad range of cortical sites and limbic structures, including the hippocampus, and are involved in stress and cognition. In particular, the hippocampus, the primary target tissue of the glucocorticoid stress hormones, is associated with cognitive function in tandem with hypothalamic-pituitary-adrenal (HPA) axis modulation. The present review summarizes glucocorticoid and HPA axis research to date in an effort to establish the manner in which stress affects the release of acetylcholine (ACh), glucocorticoids, and their receptor in the context of cognitive processes. We attempt to provide the molecular interactive link between the glucocorticoids and cholinergic system that contributes to BFCN degeneration in stress-induced acceleration of cognitive decline in aging and AD. We also discuss the importance of animal models in facilitating such studies for pharmacological use, to which could help decipher disease states and propose leads for pharmacological intervention.

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Partial loss in septo-hippocampal cholinergic neurons alters memory-dependent measures of brain connectivity without overt memory deficits

Cited by 10 publications

References 55 publications

The corticotopic organization of the human basal forebrain as revealed by regionally selective functional connectivity profiles

The corticotopic organization of the human basal forebrain as revealed by regionally selective functional connectivity profiles

The Neuroanatomy of the Reticular Nucleus Locus Coeruleus in Alzheimer’s Disease

Interaction of basal forebrain cholinergic neurons with the glucocorticoid system in stress regulation and cognitive impairment

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