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. 2017 Mar 30;322(Pt B):329-338.
doi: 10.1016/j.bbr.2016.06.056. Epub 2016 Jun 28.

Attentional updating and monitoring and affective shifting are impacted independently by aging in macaque monkeys

Daniel T Gray  1 , Anne C Smith  2 , Sara N Burke  3 , Adam Gazzaley  4 , Carol A Barnes  5
Affiliations

Attentional updating and monitoring and affective shifting are impacted independently by aging in macaque monkeys

Daniel T Gray et al. Behav Brain Res. .

Abstract

One hallmark of the normal cognitive aging process involves alterations in executive function. Executive function can be divided into at least three separable components, including set shifting, attentional updating and monitoring, and inhibition of prepotent responses. The ability to study the neural basis of cognitive aging has been enriched by the use of animal models such as the macaque monkey. In aged macaques, changes in attentional updating and monitoring systems are poorly understood compared to changes in shifting and inhibition. A partial explanation for this is the fact that the tasks designed to study executive function in aged monkeys, to date, primarily have probed shifting and inhibition processes. Here we examine how aging impacts attentional updating and monitoring processes in monkeys using an interference task designed after a paradigm used to examine multi-tasking in older humans. Young and aged macaque monkeys were tested on this interference task as well as on an object reversal learning task to study these processes in the same animals. Relative to the young monkeys, aged animals were impaired on both tasks. Proactive and retroactive interference did not differ between age groups on an array of 40 object pairs presented each day in the object reversal learning task. The levels of performance on the interference task were not correlated with levels of performance in the object reversal task. These results suggest that attentional updating and monitoring and affective shifting are separable functions in the macaque, and that normal aging affects these mental operations independently.

Keywords: Cognitive aging; Executive function; Interference; Nonhuman primate.

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Figures

Figure 1
Figure 1
Depictions of the delayed nonmatching-to-sample (DNMS) interference paradigm and the object reversal learning paradigm. A) Monkeys learned a DNMS task in a Wisconsin General Testing Apparatus (WGTA) using trial-unique objects, ensuring that the monkeys do not develop a bias towards any particular object. In the sample phase of the task, a single object is presented over the middle of three wells. A 30 second delay period follows the sample phase. During this delay a wooden guillotine door separates the animal from the wells in the testing apparatus. The test phase follows the delay. In this phase two objects, the sample object and a novel object, are presented over the lateral two wells of the apparatus. Only the novel object is baited, and the monkey must displace this object to receive food reward. After animals reach a 90% performance criterion over 5 days, three interference test conditions are implemented during the delay period of the DNMS task. B) An ‘Interruption Condition’ in which the monkey had to perform an object discrimination task during the delay, C) a ‘Relevant Distraction Condition’ in which an object could be moved to obtain a reward, and D) an ‘Irrelevant Distraction Condition’ in which an object was presented but could not be touched. E) The object reversal learning task required monkeys to learn 40 novel object pairs presented sequentially in the same order every session until they reached a 90% performance criterion (Object Discrimination). After reaching criterion, the object-reward associations were switched (Reversal Learning), and the monkeys re-learned the new associations to the same 90% criterion.
Figure 2
Figure 2
Performance on the DNMS alone condition in young and old monkeys. Boxes indicate the interquartile range (IQR) with whiskers extending to the most extreme data points that are no more than 1.5 × IQR from the edge of the box. Red line indicates median values. Grey circles are jittered so that individual animal performance scores can be more easily seen. There is no difference between age groups after reaching asymptotic behavioral levels.
Figure 3
Figure 3
Effects of irrelevant distraction, relevant distraction and interruption conditions on accuracy of choice performance on the DNMS task (Panels A, C, and E) and on reaction time (Panels B, D and F) for all animals. In all plots black circles represent individual young monkeys and light grey squares represent individual aged monkeys. All diagonal lines represent the unity line, where performance or reaction times from both conditions are equal. Note that performance and reaction time after the relevant distraction condition does not significantly deviate from the unity line in either age group (C, D). For the irrelevant and interruption conditions, performance of both young and old animals significantly deviated from the unity line (poorer performance; A, E). Reaction times in the irrelevant distraction condition were slower than in the DNMS alone condition (B), whereas reaction times in the interruption condition did not differ from the DNMS alone (F).
Figure 4
Figure 4
Example performance for one young (top row) and one aged (bottom row) monkey for the object discrimination task (left column) and reversal learning task (right column). Raw proportion of correct responses per day are shown as grey circles. Blue shaded area indicates the 90% confidence bounds for the learning curves as estimated by a state-space model. The probability of a correct response by chance is indicated by the horizontal red dashed line at 0.5. The estimated learning day (the day that performance is estimated to be more than 95% greater than chance) is indicated by numbers inside in each figure.
Figure 5
Figure 5
Estimated learning days for young and aged animals for the object discrimination and reversal learning tasks. Green circles are jittered so that individual animal performance scores can be more easily seen… Boxes indicate the interquartile range (IQR) and whiskers are extended to the most extreme data points that are no more than 1.5 × IQR from the edge of the box. Red line indicates median values. Both young and aged monkeys required more trials to reach the learning criterion in the reversal learning component of the task compared to the object discrimination component. Aged animals required more trials to reach learning criterion in both components of the task.
Figure 6
Figure 6
Comparison of learning days for old and young monkeys combined for the first 14 objects, the second 12 objects and the final 14 objects of the object pair array (40 pairs total). A) object discrimination and B) reversal learning tasks. Box and whiskers indicate the interquartile range (IQR) and the most extreme data points that are no more than 1.5 × IQR from the edge of the box, respectively. Red line indicates median values. Grey circles are jittered so that individual animal performance scores can be more easily seen. Note that in both cases, the middle third of objects were acquired faster than objects at the beginning or end of the list.
Figure 7
Figure 7
Performance on the reversal learning task compared with performance on the DNMS with interruption task. Relative impairment scores for the object reversal learning task were obtained by subtracting the learning day on the object discrimination task from the learning day on the reversal learning task (y-axis). Relative impairment scores for the DNMS with interruption task were obtained by dividing the performance on the DNMS with interruption condition by performances on the DNMS alone condition (x-axis). Young and old animals’ data are indicated with grey squares and black circles, respectively. Trend lines for the young and old data are in grey and black, respectively. Note that there is no relationship between the impairment scores on these two tasks.
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