•Assessed recognition memory in infant monkeys with neonatal perirhinal lesions using the visual paired comparison task.•Performance was assessed at 4 developmental ages.•Novelty preference ...deteriorated with age after neonatal perirhinal lesions.•Presence of functional sparing.•Memory deficits after perirhinal lesions occurred earlier than after hippocampal lesions.
To investigate the role of the perirhinal cortex on the development of recognition measured by the visual paired-comparison (VPC) task, infant monkeys with neonatal perirhinal lesions and sham-operated controls were tested at 1.5, 6, 18, and 48 months of age on the VPC task with color stimuli and intermixed delays of 10 s, 30 s, 60 s, and 120 s. Monkeys with neonatal perirhinal lesions showed an increase in novelty preference between 1.5 and 6 months of age similar to controls, although at these two ages, performance remained significantly poorer than that of control animals. With age, performance in animals with neonatal perirhinal lesions deteriorated as compared to that of controls. In contrast to the lack of novelty preference in monkeys with perirhinal lesions acquired in adulthood, novelty preference in the neonatally operated animals remained above chance at all delays and all ages. The data suggest that, although incidental recognition memory processes can be supported by the perirhinal cortex in early infancy, other temporal cortical areas may support these processes in the absence of a functional perirhinal cortex early in development. The neural substrates mediating incidental recognition memory processes appear to be more widespread in early infancy than in adulthood.
To examine the developmental trajectory of object recognition memory and its neural substrate, 10-12-d-old monkeys (Macaca mulatta) received sham operations or neurotoxic hippocampal lesions and were ...tested at the ages of 1.5, 6, and 18 months on the visual paired-comparison task using delays of 10, 30, 60, and 120 s. In sham-operated controls, incidental recognition memory was present at 1.5 months, became more robust at 6 months, and was delay-dependent by 18 months of age, suggesting that the brain structures mediating these early developing recognition abilities may undergo significant modifications after 6 months of age in monkeys. A similar developmental progression was also observed in animals with neonatal hippocampal lesions, although the delay-dependent effect at 18 months was significantly more pronounced after the neonatal hippocampal lesions, suggesting that with maturation animals with neonatal hippocampal lesions grow into a recognition-memory deficit. These findings suggest not only that the medial temporal cortical areas, known to mediate incidental recognition memory processes in adulthood, could support these processes in early infancy even when long delays are used, but also that later in development, after reaching functional maturity, the hippocampus begins to interact with the medial temporal cortical areas to mediate this function.
Recognition memory impairment after selective hippocampal lesions in monkeys is more profound when measured with visual paired-comparison (VPC) than with delayed nonmatching-to-sample (DNMS). To ...clarify this issue, we assessed the impact of stimuli similarity and encoding duration on the VPC performance in monkeys with hippocampal lesions and sham-operated controls. The novelty preference was compared for pictures of dissimilar vs. similar objects and for encoding duration of 30, 10, 5, and 1 sec. The novelty preference was spared after hippocampal lesions with dissimilar (colored or black and white BW) stimuli and an encoding time less than or equal to 10 sec, but declined with similar stimuli or a short encoding time of 1 or 5 sec. Therefore, the severe VPC impairment reported earlier after hippocampal damage cannot be attributed to the long encoding time used (30 sec) relative to DNMS (1-5 sec). However, it may result, at least in part, from the poorer distinctiveness of the stimuli typically used for VPC (BW slides of pictures of equal size and brightness of objects differing in shape) relative to the actual objects used for DNMS, differing in shape, color, size, brightness, and texture. This conclusion fits well with current models that view the hippocampus as a comparator capable of individualizing the representations of highly overlapping inputs.
▶ Aged primates have impairments in visual discrimination learning but perform well once a task is learned. ▶ Aged primates performed as well as young animals on an attention set shifting task. ▶ ...Aged primates had difficulty in inhibiting responding in a sustained attention task. ▶ In comparison to young adult animals, aged primates had greater individual variability in cognitive performance.
Understanding how cognition declines in normal aging is vital in order to distinguish between normal cognitive decline due to aging and cognitive decline due to an age-related pathological process such as Parkinson's disease (PD). Several cognitive domains including memory, executive functioning and attention are all adversely affected with age in humans, as well as by PD, yet less is known about how these processes are affected by aging in non-human primates. Thus, in order to characterize baseline performance in aged primates prior to inducing Parkinson-like pathology, male rhesus macaques aged 15–22 years were tested on several tasks analogous to those used in cognitive aging studies in humans. The tasks included simple visual discrimination to assess learning and reference memory, discrimination reversal to assess cognitive flexibility and response inhibition, continuous performance to assess sustained visual attention, and attention set shifting to assess cognitive flexibility and set-shifting ability. Deficits were detected in some aspects of learning, cognitive flexibility, response inhibition and sustained visual attention, whereas reference memory and set-shifting did not appear to be affected. Additionally, there was a greater amount of variability in cognitive abilities across the aged animals than observed previously in young adult animals. These findings will form an important baseline for comparison with cognitive performance after PD-like pathology is superimposed on the normal aging process.
► Aged primates are impaired in spatial working memory (SWM) learning and performance. ► Difficulty in learning a SWM task can be improved by manipulating task variables. ► Stimuli locations, ...repetition rate and inter-trial interval influence learning.
Aged non-human primates may have deficits in a variety of cognitive functions. However, it is possible that at least some age-related performance deficits relate to a deficit in initial task learning. To assess this, aged rhesus monkeys were trained to perform a Self-Ordered Spatial Search (SOSS) task using the same training and testing parameters used previously with normal young animals. Aged animals failed to reach criterion at the easiest task level. In an attempt to improve learning, a group of aged animals were first trained on SOSS using a standard 5s ITI, followed by trials with low inter-trial interference (e.g., a stimulus used in a trial would not be used again for the next 2 trials) or with trials in which the spatial distance between the stimuli on the screen was maximized. Because performance improved but failed to reach criterion, this was followed by sessions with increasing ITIs (from 5s to 10 or 15s). Only increasing the ITI improved the performance of the aged animals enough to allow them to learn the task to criterion. Once the criterion was reached, memory was taxed by increasing the delay between stimulus presentations and increasing the number of spatial positions to be remembered. Performance declined for young animals, but even more so for aged animals. The results of the present study suggests that aged primates have difficulty initially learning a complex working memory task, and that the ITI may be an important parameter to manipulate to improve learning. However, once the task is learned, performance of aged animals is inferior to that of young animals, particularly when memory demands are increased.
Object recognition memory as assessed by the visual paired comparison task (VPC) is known to emerge early in infancy in both human and non-human primates. However, neither the normal maturation of ...these processes, nor the developmental role of the medial temporal lobe structures thought to be involved in this form of incidental memory have been systematically examined through longitudinal studies. Therefore, this study longitudinally followed the normal maturation (Group Neo-C) of recognition memory processes as well as measured the magnitude of object recognition memory deficits seen after selective neonatal hippocampal (Group Neo-H) or perirhinal cortex (Group Neo-PRh) damage in monkeys (Macaca mulatta). The data showed that (1) incidental recognition emerges very early in life and, at this early age, is mediated by PRh rather than H; (2) this memory process, however, proceeds through major maturational changes after the first year of life, presumably as H becomes functional and begins competitive functional interactions with PRh; (3) equally interesting was that, although Neo-PRh lesions impacted item-specific recognition memory at all ages tested so far (1.5-18 months), this impairment was less in magnitude than that reported after PRh lesions in adulthood, suggesting that the neural substrate mediating incidental recognition memory in early infancy is more widespread than that of the adult. However, this proposal warrants further investigation since it is uncertain as yet whether performance of animals with Neo-PRh damage will worsen with age to reach the magnitude seen with adult PRh lesions or whether developmental plasticity will further ameliorate their deficit. Finally, the data obtained in these developmental studies provide further support to the idea that the recognition processes mediated by the perirhinal cortex are different from those supported by the hippocampal formation.
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