This finding indicates a cross-species similarity in this age-associated hyperexcitability between rats and humans (15, 16). Author contributions: D.T.G. This circuitry is described here in the context of a two-level model that distinguishes between feedforward and feedback connections. Animal models of cognitive and sensory aging have enriched our understanding of the mechanisms that contribute to different aspects of healthy brain aging. This is largely due to evidence from large longitudinal studies that individuals with poorer acoustic function are at a higher risk of developing age-related cognitive decline and dementia (83, 84). Macaques with object recognition memory deficits display hyperactivity in the CA3 region of the hippocampus that is associated with fewer somatostatin(SOM)-positive inhibitory interneurons. Greater numbers of neurons expressing CaBPs in the central auditory system of aging macaques is associated with poorer peripheral auditory function. “This would pave the way for a similar stimulation paradigm to be used in the clinic,” said Redinbaugh. The brains from these animals were then harvested and serially sectioned for immunohistochemical labeling of 2 chemically distinct classes of inhibitory cells: somatostatin-positive and parvalbumin-positive interneurons. “Achieving this goal will allow us to better understand the mechanisms of general anesthesia and the impacts of brain trauma, [and also] target clinical interventions to improve the lives of patients who suffer from disorders of consciousness, such as coma,” she told Gizmodo. Conversely, parvalbumin-positive interneuron numbers did not change with age, and they were not associated with firing rates or object recognition memory abilities. There will be a particular emphasis on conceptualizing the critical bridge that nonhuman primates provide between behavioral, neuroanatomical, and electrophysiological data obtained in aged rodents and cognitive, psychophysical, and functional imaging data from older humans. 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Jaan Aru, a neuroscientist at Humboldt University in Berlin, said researchers in the 1990s began to think that the thalamus was important for consciousness—a belief predicated on the fact that the thalamus is located in a central position for control and that it can change how other brain regions process information. This work was supported by NIH Grants R01 AG050548 (to C.A.B.) A critical aspect of the experiment was to correctly evaluate wakefulness in the two monkeys used in the experiment, dubbed Monkey R and Monkey W. “We modeled our assessment of wakefulness in monkeys on clinical measures that are used to assess coma patients or patients that are undergoing anesthesia,” Redinbaugh told Gizmodo. Whether the reduction observed reflects cellular degeneration or a biochemical down-regulation of the neuropeptide somatostatin remains an open question. In this study, we applied both histone demethylase Kdm4d mRNA and histone deacetylase inhibitor trichostatin A (TSA) to the cloning of macaque monkeys. Adapted by permission from ref. We present a quadrature volume coil designed for brain imaging of a macaque monkey fixed in a sphinx position (facing down the bore) within a stereotactic frame at 3 T, where the position of the monkey and presence of the frame preclude use of existing coils. The acquisition of multiple estimates of cognitive and sensory function within the same group of monkeys allowed an assessment of whether specific cognitive and sensory domains changed independent of one another or in tandem (90). Recent work utilizing aging macaques provides a perspective on the association between auditory and cognitive function across the lifespan (90). The technology could one day make artificial eyesight possible in humans. Consequently, age-related deficits in human episodic memory are thought to largely result from structural and functional alterations in these structures, although the precise neurobiological mechanisms involved have been difficult to pinpoint. A rhesus macaque. In short, Little Dog says, macaque monkeys “employ memory … 5B) and lower acoustic thresholds (Fig. Furthermore, cognitive and sensory brain structures in nonhuman primates share many more organizational principles with human brains than do the brains of phylogenetically more distant laboratory animals such as rodents (7⇓⇓⇓–11) (Fig. Note that both auditory brainstem response thresholds and hair cell numbers reflect cochlear function. Since the 2000s, however, neuroscientists have focused primarily on the cortex to find the mechanisms of consciousness, he said. Non-human primates like the macaque are able to communicate about such things as food, identity or danger with vocalizations that are interpreted by others of their species and acted upon. (B) Animals with higher right hemisphere fimbria-fornix FA had better auditory processing abilities. When contemplating the coos and screams of a fellow member of its species, the macaque uses brain regions that correspond to the two principal language centers in the human brain. Recent public concern about nonhuman primate research has made it imperative to attempt to clearly articulate the potential benefits to human health that this model enables. Anatomical differences like these highlight the fact that sensory systems develop to process species-relevant information, and that differences in sensory transduction ranges will be reflected in the basic structure of an animal’s nervous system. Audiometric deficits can result from various insults to the cochlea that diminish this sensory organ’s capacity to transduce acoustic information (44⇓⇓–47). PRC firing rates were not different between age groups. … Note that lower values indicate better function for both auditory measures. Parvalbumin-positive neuron density was not different between age groups in either region. Both of these points emphasize how nonhuman primates can provide a fundamental link between nonprimate laboratory animals and humans. One important translational implication of this work is the suggestion that age-related episodic memory decline may be alleviated by manipulating the function of specific interneuron subtypes to rebalance local network activity. Additionally, axospinous, axosomatic, and axodendritic spine sizes appear to increase with age in the prefrontal cortex, and the extent of these structural changes in superficial cortical layers was significantly associated with performance measures on an object recognition task (36, 37). It becomes especially critical to use animal models that possess brains with chemical compositions similar to those of humans when potential therapies depend on targeting genetically defined cell types. Baseline firing rates were significantly greater in the CA3 of aged animals relative to the adults. Lesion and functional imaging studies in humans indicate that the integrity of medial temporal lobe brain structures, including the hippocampus, is critical for episodic memory formation (13, 14). Because cognitive problems arise relatively late in the progression of these diseases, some participants considered to be aging normally may actually have undetected pathophysiological brain markers during the period when behavioral testing is conducted (5). Little Dog claims that the brain of a macaque monkey is closer to a human brain than any other living mammal, and he claims that the macaques are capable of critical thought and problem solving, and that they have the ability to recall past events. For example, intracellular recordings indicate that pyramidal neurons in the lateral prefrontal cortex become more excitable with age, as reflected by increases in membrane input resistance and action potential discharge to a given stimulation intensity (41). Diffusion tensor … These measures included such things as the monkeys opening their eyes, making purposeful reaches, moving their faces, and showing responsiveness to touch, explained Redinbaugh. The brains of the monkeys are considered a delicacy, and they are thought to be a cure for impotence. (D) Representative probability map of the right hemisphere frontal thalamic radiation overlaid upon T1-weighted MRI (Top) and an FA map pseudocolored in copper (Bottom). Online ISSN 1091-6490. Another observation in hippocampal circuits of aged rats is that there are significantly fewer inhibitory cells both within CA3 and the hilar region of the dentate gyrus compared with younger animals (25). The present review will highlight how nonhuman primates provide a critical bridge between experiments conducted in rodents and development of therapeutics for humans. Thus, the striking specificity by which anatomical connectivity, auditory physiology, and cognitive outcome measures covaried across the lifespan in this study indicates that normative aging impacts neural networks contained within the temporal lobe more similarly than circuits residing in other brain regions (i.e., between the frontal and temporal lobes in this study). These data also provide a possible mechanistic explanation for the excitability observed at the single-cell level in aged rats and in fMRI studies in older humans. Schematic depiction of the relative size of auditory nuclei within the SOC of humans, macaques, and rats. Sensory functioning and intelligence in old age: A strong connection, The strong connection between sensory and cognitive performance in old age: Not due to sensory acuity reductions operating during cognitive assessment. These observations indicate that the neurobiological processes driving functional changes in aged cognitive circuits (e.g., hyperexcitability) likely occur at subcellular levels. Visual information processing and auditory thresholds were not associated with any aspect of cognition tested. To that end, Redinbaugh, along with senior author Yuri Saalmann and their colleagues, devised an experiment with the intent of inducing consciousness in anesthetized subjects. Are age-related changes in cognitive function driven by age-related changes in sensory processing? Importantly, this study also demonstrated that the extent of CA3/dentate gyrus hyperactivation was significantly associated with discrimination abilities in these participants, regardless of age (15). Comparison of human, macaque, and mouse brains. E.A.B. This paper results from the Arthur M. Sackler Colloquium of the National Academy of Sciences, “Using Monkey Models to Understand and Develop Treatments for Human Brain Disorders,” held January 7–8, 2019, at the Arnold and Mabel Beckman Center of the National Academies of Sciences and Engineering in Irvine, CA. More recently, the impact that hearing loss, in particular, has on cognition has reemerged as a topic of research interest. This similarity in cortical function between humans and old-world monkeys suggests that brain networks supporting volitional communication have a common evolutionary origin that arose well prior to the hominin radiation. Tetrode recording probes were advanced individually with a hyperdrive device that allowed the acquisition of single action potentials from hippocampal CA3 pyramidal cells at more superficial depths. Leslie G. Ungerleider, NIMH-NIH "This is an extraordinarily detailed and comprehensive atlas of the macaque monkey brain. One location along the ascending auditory pathway where these interspecies differences are clear is within the superior olivary complex (SOC) in the ventral brainstem. NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. Together, these findings suggest that age-associated changes in hippocampal inhibitory circuits may lead to CA3 hyperexcitability and circuit dysfunction that impacts memory. Among others, 2 differences will be discussed here: 1) distinct CaBP expression patterns of auditory neurons and 2) distinct hearing ranges between rodents and macaques. With respect specifically to a calcium homeostasis approach, there is evidence that CaBP expression differs considerably between the auditory systems of primates and rodents. The data discussed here do not focus on age-associated changes in the cochlea, but rather on the central auditory system’s response to a weakened drive from the periphery. When the tetrodes were advanced further into the brain, perirhinal cortical cells were also recorded. I mean, side-effects aside, of course. Emergence of a powerful connection between sensory and cognitive functions across the adult life span: A new window to the study of cognitive aging? 58. Observations of central auditory system hyperexcitability led to the hypothesis that some aspects of presbycusis may result from altered calcium dynamics in aged auditory neurons that could lead to cell dysfunction and excitotoxicity that disrupts network function. 1). Importantly, the number of a specific type of interneuron expressing the neuropeptide somatostatin was positively associated with memory function in aged rats (25). As a result, histological experiments aimed at quantifying the number of neurons expressing calcium binding proteins (CaBPs) were conducted throughout the central auditory system. The macaques constitute a genus of gregarious Old World monkeys of the subfamily Cercopithecinae. 2D). In terms of the ethics involved, “University of Wisconsin-Madison Institutional Animal Care and Use Committee approved all procedures, which conformed to the National Institutes of Health Guide for the Care and Use of Laboratory Animals,” the authors wrote in the paper. (B) Coronal Nissl-stained sections of hippocampus-containing tissue in the 3 species. (Bottom) Rats, on the other hand, have a drastically expanded LSO relative to humans and macaques, as well as a significantly reduced MSO. NAS colloquia began in 1991 and have been published in PNAS since 1995. Critically, there was a selective decrease in somatostatin-positive interneuron density in the stratum oriens layer of CA3 (Fig. What that in mind, the new research could result in effective new therapies to treat disorders of consciousness, improved deep brain stimulation as a surgical technique, and better drugs for anesthesia. In particular, superior auditory processing was associated with better performance on tests of concurrent reversal learning, object recognition memory, and discrimination of objects with high feature overlap, but not with performance on tests of reward devaluation, spatial short-term memory, or object discrimination. I’d absolutely be down for a brain implant that I could switch myself off like a light by stimulating the thalamus at a different frequency, then waking myself up. These findings indicate that aging can lead to a disruption in the activity of circuits within the hippocampus that negatively impacts mnemonic processing. Insights into these basic questions are critical for devising strategies to maintain cognitive health in older individuals who fall along all points of the sensory and cognitive aging spectrum. The June 2018 release is out. While fMRI technologies can detect broad changes in activity, they do not provide detailed circuit-level insights into such changes. Copyright © 2021 National Academy of Sciences. Adult and aged macaques completed a battery of behavioral tests designed to probe the function of distinct aspects of frontal and temporal lobe-dependent cognition. (A) Images of the dorsal surface of a human brain, macaque brain, and mouse brain. “I hope many studies will follow that will try to better understand the role of thalamus not only in the state of consciousness, but also in perceptual processes.”. So far, evidence for a similar network in monkeys is mainly indirect, since, except for one positron emission tomography study, it is all based on functional connectivity analysis rather than activity increases during passive task states. This physiological change would be expected to combine with known age-associated increases in L-type calcium channel conductance and calcium release from intracellular stores to result in higher calcium levels in hippocampal neurons of aged rats (19⇓⇓–22). (B) Age is significantly associated with greater numbers of auditory neurons expressing parvalbumin in the core of the inferior colliculus (IC). By experimenting on macaque monkeys, researchers from the University of Wisconsin-Madison have uncovered new evidence affirming the central lateral thalamus as an NCC. Furthermore, these electrophysiological changes were significantly associated with performance on an object recognition task (41). To do so, they designed a stimulation method that mimicked the way brain cells act in the central lateral thalamus during the waking state. This would be fantastic if it led to advances in the areas of insomnia and narcolepsy. By experimenting on macaque monkeys, researchers from the University of Wisconsin-Madison have uncovered new evidence affirming the central lateral thalamus as an NCC. (C) Animals with more parvalbumin-positive cells in the IC had higher auditory brainstem response pure-tone average thresholds. Additionally, both within and between brain regions, aged neurons can exhibit striking differences in excitability. The study was conducted in macaque monkeys. 4). Animals with greater hippocampus-associated white matter integrity have better auditory processing capacities and lower auditory thresholds. 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