Once the stimulation was turned off, the macaques returned to an unconscious state. 5A) and hippocampal commissure, both fiber tracts associated with hippocampus connectivity, were better able to discriminate stimuli with overlapping features, a cognitive process known to require medial temporal lobe circuits. In macaques, 2 parallel ascending pathways that can be distinguished by immunohistochemical labeling of the CaBPs parvalbumin and calbindin traverse through the auditory system. D, dorsal; L, lateral; M, medial; V, ventral. The technology could one day make artificial eyesight possible in humans. Comparative approaches to understanding brain aging in humans, using nonhuman primates, will be critical for gaining a more complete understanding of the fundamental principles by which neuronal networks compensate for and adapt to patterns of functional decline that arise uniquely in older individuals. Finally, another possibility is that the extent of neuronal connectivity between regions may determine the degree to which brain functions covary across the lifespan through mechanisms associated with hyperexcitability or changes in synaptic function. Distinguishing similar, but nonidentical, experiences is a critical aspect of episodic memory that commonly becomes impaired in older individuals (16). Animals were euthanized first by sedation using ketamine and dexdomitor, followed by deep anesthetization using pentobarbital and phenytoin, and then were perfused transcardially with 4% (wt/vol) paraformaldehyde in phosphate buffer. 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). 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. Face recognition and the interpretation of facial expressions and gaze direction play a key role in guiding the social behavior of human beings, and new study results point to similar mechanisms in macaques. In awake macaques, prefrontal cortical neurons show reduced firing rates (42), whereas temporal lobe neurons recorded in the CA3 region show increased excitability (27), but hippocampal granule cells recorded in vitro show no change in firing rate (43). It seems like the definition of inhumanity,…. A major goal within the field of the neuroscience of aging is to determine what factors allow certain individuals to evade neurodegenerative disease, while others succumb to them. 5C). Three rhesus macaques (1 male, 2 females, 4–6 kg, 8–9 years of age) were tested. (Middle) Organization of the macaque SOC follows very similar organizational principles, with a slightly larger LSO and slightly smaller MSO than humans. Adapted by permission from ref. Although the evidence is still limited, a growing body of research suggests music may have beneficial effects for diseases such as Parkinson’s. One often misunderstood aspect of the normative brain aging process is that while an enormous absolute number of individuals present with a dementing neurodegenerative disease at some time in their life (14% of people over the age of 70 y), the vast majority of people (86%) take healthier cognitive trajectories (2). Extracellular recordings across various hippocampal subfields have shown that neurons specifically in the CA3 region become hyperexcitable (higher firing rates) in older animals, whereas CA1 pyramidal cell firing rates are not different between adult and aged rats (17). Thank you for your interest in spreading the word on PNAS. (E) Frontal radiation FA was not associated with auditory processing. While fMRI technologies can detect broad changes in activity, they do not provide detailed circuit-level insights into such changes. Because the impact that age will have on a specific neural network cannot necessarily be predicted a priori, it is essential to examine regions independently as age-related changes in one circuit may not generalize to those observed in another. 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. Greater numbers of neurons expressing CaBPs in the central auditory system of aging macaques is associated with poorer peripheral auditory function. (A) Images of the dorsal surface of a human brain, macaque brain, and mouse brain. Nonhuman animals also do not spontaneously develop dementing neurodegenerative diseases, which eliminates a major confound often encountered in human brain aging research. In this study, we use the intricate connections of frontal, cingulate, and parietal areas, well established by the anatomical literature, to derive a symmetrical histological connectivity matrix composed of 59 cortical areas. Under this hypothesis, the efficacy of neural circuits in relatively close proximity might become similarly impacted by vascular aging. Parvalbumin-positive neuron density was not different between age groups in either region. Stimulating this small brain region, which is located deep in the forebrain, caused anesthetized monkeys to suddenly wake up and be alert, despite the fact that anesthetic drugs were still being administered. The study was conducted in macaque monkeys. Perhaps the most important interspecies difference between rodents and primates with respect to presbycusis research is their vastly different hearing ranges. The June 2018 release is out. For example, a generational effect sometimes encountered in human cognitive neuroscience is differential exposure to technology, such as expertise with computers, between generations that can cause older individuals to perform more poorly than younger people on tasks, regardless of their actual cognitive status (6). The results discussed here call for a shift in focus in cognitive aging research toward understanding how different brain functions impact one another across a lifespan. Critically, there was a selective decrease in somatostatin-positive interneuron density in the stratum oriens layer of CA3 (Fig. While cortical neurons are not lost with age, unbiased stereological assessments indicate that there is a 30 to 60% decrease in prefrontal cortical synapse density with age (34), and that both excitatory and inhibitory synapses are vulnerable (35). Hippocampal synapse density has also been carefully examined across the macaque lifespan, with the bulk of this work focusing on synapses formed by perforant path input from the superficial layers of the entorhinal cortex to the inner and outer molecular layers of the dentate gyrus (38). 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. What’s more, the findings could take us closer to understanding consciousness itself. An absolute must for all neuroscientists navigating the rhesus monkey brain."--Dr. 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. New research suggests monkeys, like this Japanese macaque, have vocal tracts anatomically capable of humanlike speech, but they lack the necessary brain wiring to produce it. During the experiment, the scientists attempted to stimulate various parts of the deep brain, but none elicited the same response as the central lateral thalamus, which emerged a kind of consciousness hotspot in the brain. (A) Photomicrographs of parvalbumin-expressing neurons in an adult and aged macaque auditory brainstem. 58; and 59, which is published under CC BY 3.0. Schematic depiction of the relative size of auditory nuclei within the SOC of humans, macaques, and rats. Second, differential patterns of age-related neurovascular dysfunction between different brain regions also could bias circuits contained within a lobe to experience comparable physiological consequences associated with poorer vascular health. New research published today in Neuron takes us a small but important step closer to the answer. Unlike in the prefrontal cortex, the density of axospinous synapses, which are the predominant synapse type in the dentate gyrus, remains stable across the macaque lifespan (39, 40). More recently, the impact that hearing loss, in particular, has on cognition has reemerged as a topic of research interest. 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). Macaque monkeys, in particular, have been the predominant nonhuman primate model in neuroscience, although relatively recent advances in transgenic technologies for use in marmosets (99⇓–101) have rapidly established this anthropoid as a promising additional nonhuman primate tool. “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.”. 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. Importantly, auditory processing abilities were not associated with the microstructural condition of white matter in the frontal thalamic radiations (Fig. 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. Interaural time differences are the primary cue used to localize lower frequency sounds, and these computations primarily involve the medial superior olivary (MSO) nucleus (74, 75). (B) Age is significantly associated with greater numbers of auditory neurons expressing parvalbumin in the core of the inferior colliculus (IC). Macaque monkeys have become the predominant nonhuman primate model system in brain aging research due to their striking similarities to humans in their behavioral capacities, sensory processing abilities, and brain architecture. Both of these points emphasize how nonhuman primates can provide a fundamental link between nonprimate laboratory animals and humans. A strong argument can be made that, despite the measures taken, the animals did suffer during this experiment and that monkeys should never be used for experiments such as this. Functional anatomical work has shown that neurons belonging to each pathway participate in vastly different aspects of acoustic processing, with the parvalbumin-rich direct pathway primarily acting as an information-relay system and the calbindin-rich indirect pathway acting more as a modulator (68). An important clue to a critical brain change that occurs in aging came from a study that used functional magnetic resonance imaging (fMRI) to demonstrate that the CA3/dentate gyrus region of the hippocampus is more active in older individuals than in younger adults as they attempt to discriminate increasingly overlapping visual stimuli (15). In particular, this review will highlight studies that have utilized aged macaques to gain network-level and regional insights into age-related episodic memory decline and hearing loss, which are 2 of the most commonly experienced alterations in brain function experienced by older individuals. 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. Together, these diffusion tensor imaging data indicate that auditory processing abilities and medial temporal lobe-dependent cognition become associated across an animal’s lifespan due, in part, to differential structural alterations to white matter in the temporal versus frontal lobes. Critically, rodents do not appear to have these chemically defined parallel auditory pathways since the auditory thalamus of rats is almost completely devoid of parvalbumin and lacks calbindin in many areas where it is clearly expressed in primates (69, 70). 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. 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. (C) Magnified images of CA3 and PRC SOM inhibitory neurons. Reprinted with permission from ref. 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. These findings indicate that aging can lead to a disruption in the activity of circuits within the hippocampus that negatively impacts mnemonic processing. Nonhuman primates provide the animal model that is closest to humans and remain an important bridge for testing the veracity of discoveries effective in rodents when clinical applications of these are being considered for human testing. Comparison of human, macaque, and mouse brains. Despite evidence dating back several decades to suggest that individuals with poorer sensory function are more likely to have cognitive problems later in life, the neurobiological processes responsible for these associations have not been a subject of intense research (79⇓⇓–82). 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. 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Superior auditory processing, however, was related to better overall cognitive function. Are age-related changes in cognitive function driven by age-related changes in sensory processing? (Top) Human SOC is characterized by a relatively small LSO nucleus (light blue) and an elongated MSO nucleus that is surrounded by other olivary nuclei (gray). Since the 2000s, however, neuroscientists have focused primarily on the cortex to find the mechanisms of consciousness, he said. The brains were extracted and … Contribution of frontal and temporal lobe function to memory interference from divided attention at retrieval, Age-related impairment in executive functioning: Updating, inhibition, shifting, and access. Baseline firing rates were significantly greater in the CA3 of aged animals relative to the adults. Looking ahead, Redinbaugh said that, since her team now has a method to finely manipulate consciousness, they can test predictions of the major theories of consciousness, “which differ with respect to the brain areas that are most important for consciousness.” They also plan to stimulate a fuller range of areas in the thalamus and determine which frequencies are most effective in influencing consciousness. Nobody likes the idea of experimenting on animals. (Scale bar, 100 μm.) Furthermore, these electrophysiological changes were significantly associated with performance on an object recognition task (41). This observation highlights a major challenge in cognitive aging research of understanding each individual’s unique behavioral and neurobiological profile. Together, these observations indicate that auditory processing abilities functionally covary specifically with aspects of cognition driven by medial temporal lobe networks, regardless of auditory acuity. 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