Reduction in hippocampal cholinergic innervation is unrelated to recognition memory impairment in aged rhesus monkeys

Calhoun, Michael E.; Mao, Ying; Roberts, Jeffrey A.; Rapp, Peter R.

doi:10.1002/cne.20181

Cited by 45 publications

(36 citation statements)

References 48 publications

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“…During normal aging, the volume of the hippocampus (total or any of its subfields) remains stable in rhesus monkeys (Peters et al 1996;Calhoun et al 2004;Shamy et al 2006Shamy et al , 2010Makris et al 2010). This is in contrast to a substantial number of MRI studies reporting a reliable age-related decline in hippocampal volume in healthy humans (Kaye et al 1997;Mueller et al 1998;Tisserand et al 2000;Raz et al 2004;Walhovd et al 2009).…”

Section: Gross Anatomy Of Hippocampal and Related Cortical Regionsmentioning

confidence: 89%

“…In the DG, CA2/3, and CA1, the length of cholinergic fibers decreases with age, but this age-related decline does not correlate with recognition memory deficits as measured by DNMS scores (Calhoun et al 2004). Despite converging evidence for age-dependent vulnerability of the cholinergic system, the decline in hippocampal cholinergic innervation is not sufficient to account for DNMS impairment (Calhoun et al 2004). Thus, the functional and cognitive consequences of these morphological changes remain to be defined.…”

Section: Acetylcholinementioning

confidence: 97%

“…More recently, vesicular acetylcholine transporter immunolabeling and an unbiased stereological technique were used to estimate total cholinergic fiber length in hippocampal subregions of behaviorally characterized young and aged rhesus monkeys (Calhoun et al 2004). In the DG, CA2/3, and CA1, the length of cholinergic fibers decreases with age, but this age-related decline does not correlate with recognition memory deficits as measured by DNMS scores (Calhoun et al 2004).…”

Section: Acetylcholinementioning

confidence: 99%

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Neuronal and morphological bases of cognitive decline in aged rhesus monkeys

Hara

Rapp

Morrison

2011

AGE

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121

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Rhesus monkeys provide a valuable model for studying the basis of cognitive aging because they are vulnerable to age-related decline in executive function and memory in a manner similar to humans. Some of the behavioral tasks sensitive to the effects of aging are the delayed response working memory test, recognition memory tests including the delayed nonmatching-to-sample and the delayed recognition span task, and tests of executive function including reversal learning and conceptual set-shifting task. Much effort has been directed toward discovering the neurobiological parameters that are coupled to individual differences in age-related cognitive decline. Area 46 of the dorsolateral prefrontal cortex (dlPFC) has been extensively studied for its critical role in executive function while the hippocampus and related cortical regions have been a major target of research for memory function. Some of the key age-related changes in area 46 include decreases in volume, microcolumn strength, synapse density, and α1-and α2-adrenergic receptor binding densities. All of these measures significantly correlate with cognitive scores. Interestingly, the critical synaptic subtypes associated with cognitive function appear to be different between the dlPFC and the hippocampus. For example, the dendritic spine subtype most critical to task acquisition and vulnerable to aging in area 46 is the thin spine, whereas in the dentate gyrus, the density of AGE (2012) large mushroom spines with perforated synapses correlates with memory performance. This review summarizes age-related changes in anatomical, neuronal, and synaptic parameters within brain areas implicated in cognition and whether these changes are associated with cognitive decline.

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Section: Gross Anatomy Of Hippocampal and Related Cortical Regionsmentioning

confidence: 89%

Section: Acetylcholinementioning

confidence: 97%

Section: Acetylcholinementioning

confidence: 99%

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Neuronal and morphological bases of cognitive decline in aged rhesus monkeys

Hara

Rapp

Morrison

2011

AGE

Self Cite

121

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“…A higher density of acetyl cholinesterase has been reported in the rostral hippocampus (Rosene and Van Hoesen, 1987). Additionally, when considering the extent to which cholinergic fiber density and loss are evident in hippocampal subfields, a study based on non-human primates reported that there is a higher density in CA3 as compared to dentate gyrus and CA1, though loss of cholinergic innervation in aging is consistent across the longitudinal axis of the hippocampus (Calhoun et al, 2004). CA1 and CA3 have been found to lie primarily within the hippocampal head, and the dentate gyrus primarily within the hippocampal body in humans (Malykhin et al, 2010), which together with the aforementioned data further suggest there is increased cholinergic activity within the head of the hippocampus as compared to the body and tail, and loss of these fibers in AD may contribute to a decline in memory.…”

Section: Discussionmentioning

confidence: 99%

Hippocampal Subregions are Differentially Affected in the Progression to Alzheimer's Disease

Greene

Killiany

2011

The Anatomical Record

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Atrophy within the hippocampus (HP) as measured by magnetic resonance imaging (MRI) is a promising biomarker for the progression to Alzheimer's disease (AD). Subregions of the HP along the longitudinal axis have been found to demonstrate unique function, as well as undergo differential changes in the progression to AD. Little is known of relationships between such HP subregions and other potential biomarkers, such as neuropsychological (NP), genetic, and cerebral spinal fluid (CSF) beta amyloid and tau measures. The purpose of this study was to subdivide the hippocampus to determine how the head, body, and tail were affected in normal control, mild cognitively impaired, and AD subjects, and investigate relationships with HP subregions and other potential biomarkers. MRI scans of 120 participants of the Alzheimer's Disease Neuroimaging Initiative were processed using FreeSurfer, and the HP was subdivided using 3D Slicer. Each subregion was compared among groups, and correlations were used to determine relationships with NP, genetic, and CSF measures. Results suggest that HP subregions are undergoing differential atrophy in AD, and demonstrate unique relationships with NP and CSF data. Discriminant function analyses revealed that these regions, when combined with NP and CSF measures, were able to classify by diagnostic group, and classify MCI subjects who would and would not progress to AD within 12 months. Anat Rec,

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“…Axon length was assessed using the SpaceBalls probe under Koehler illumination at 63x (Zeiss PlanAchromat, N.A. 1.4) (Calhoun and Mouton, 2000;Mouton et al, 2002;Calhoun et al, 2004;Kreczmanski et al, 2005). SpaceBalls is a stereological tool that places sampling hemispheres for lineal features in the context of a fractionator sampling scheme (Mouton, 2002).…”

Section: Axon Length Densitymentioning

confidence: 99%

Cortical dopaminergic innervation among humans, chimpanzees, and macaque monkeys: A comparative study

et al. 2008

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In this study, we assessed the possibility that humans differ from other primate species in the supply of dopamine to the frontal cortex. To this end, quantitative comparative analyses were performed among humans, chimpanzees, and macaques using immunohistochemical methods to visualize tyrosine hydroxylase-immunoreactive axons within the cerebral cortex. Axon densities and neuron densities were quantified using computer-assisted stereology. Areas 9 and 32 were chosen for evaluation due to their roles in higher-order executive functions and theory of mind, respectively. Primary motor cortex (area 4) was also evaluated because it is not directly associated with cognition. We did not find an overt quantitative increase in cortical dopaminergic innervation in humans relative to the other primates examined. However, several differences in cortical dopaminergic innervation were observed among species which may have functional implications. Specifically, humans exhibited a sublaminar pattern of innervation in layer I of areas 9 and 32 that differed from that of macaques and chimpanzees. Analysis of axon length density to neuron density among species revealed that humans and chimpanzees together deviated from macaques in having increased dopaminergic afferents in layers III and V/VI of areas 9 and 32, but there were no phylogenetic differences in area 4. Finally, morphological specializations of axon coils that may be indicative of cortical plasticity events were observed in humans and chimpanzees, but not macaques. Our findings suggest significant modifications of dopamine's role in cortical organization occurred in the evolution of the apes, with further changes in the descent of humans.

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Reduction in hippocampal cholinergic innervation is unrelated to recognition memory impairment in aged rhesus monkeys

Cited by 45 publications

References 48 publications

Neuronal and morphological bases of cognitive decline in aged rhesus monkeys

Neuronal and morphological bases of cognitive decline in aged rhesus monkeys

Hippocampal Subregions are Differentially Affected in the Progression to Alzheimer's Disease

Cortical dopaminergic innervation among humans, chimpanzees, and macaque monkeys: A comparative study

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