Greater dependence on working memory and restricted familiarity in orangutans compared with rhesus monkeys

The prefrontal cortex is larger than would be predicted by body size or visual cortex volume in great apes compared with monkeys. Because prefrontal cortex is critical for working memory, we hypothesized that recognition memory tests would engage working memory in orangutans more robustly than in rhesus monkeys. In contrast to working memory, the familiarity response that results from repetition of an image is less cognitively taxing and has been associated with nonfrontal brain regions. Across three experiments, we observed a striking species difference in the control of behavior by these two types of memory. First, we found that recognition memory performance in orangutans was controlled by working memory under conditions in which this memory system plays little role in rhesus monkeys. Second, we found that unlike the case in monkeys, familiarity was not involved in recognition memory performance in orangutans, shown by differences with monkeys across three different measures. Memory in orangutans was not improved by use of novel images, was always impaired by a concurrent cognitive load, and orangutans did not accurately identify images seen minutes ago. These results are surprising and puzzling, but do support the view that prefrontal expansion in great apes favored working memory. At least in orangutans, increased dependence on working memory may come at a cost in terms of the availability of familiarity.

The prefrontal cortex is critical for a suite of cognitive control processes that are conspicuous in human cognition (Miller 2000; Rougier et al. 2005; Braver et al. 2009). One such process is working memory, which actively maintains representations in a state of heightened access for further processing (Baddeley and Hitch 1974; Engle 2010). Working memory and cognitive control are positively correlated with measures of general intelligence in humans, implicating the prefrontal cortex as a key neural structure in the evolution of human cognition (Gray et al. 2003; Unsworth and Engle 2007; Cole et al. 2012). Some neuroanatomical studies have found that the prefrontal cortex is larger than would be predicted based on body size and visual cortex volume in apes compared with monkeys (Rilling 2006; Passingham and Smaers 2014). These findings suggest that the prefrontal cortex expanded disproportionately in great apes during primate evolution. Disproportionate expansion of the prefrontal cortex in great apes may have resulted in greater capacity for cognitive control functions, such as working memory, compared with monkeys. Thus, studies directly comparing working memory in monkeys and apes are critical to understanding the evolution of intelligence in primates.The role of cognitive control, and thus the prefrontal cortex, varies among memory systems. For instance, working memory relies heavily on cognitive control, consuming substantial cognitive resources, and is known to depend on frontal brain areas (Goldman-Rakic 1995; Fuster 1997). In contrast, familiarity, which is a strength-based memory signal that codes for whether or not a percept has previously been experienced (Kelley and Jacoby 1998; Yonelinas 2002), relies substantially less on cognitive control, consumes fewer cognitive resources, and has been mostly associated with nonfrontal areas of the brain such as the perirhinal cortex (Bachevalier and Mishkin 1986; Brown and Aggleton 2001; Haskins et al. 2008; Tu et al. 2011; O''Neil et al. 2012). Thus, working memory and familiarity vary in the degree to which they rely on cognitive control, and the degree to which they rely on prefrontal areas of the brain.If a relatively large prefrontal cortex enhances cognitive control and working memory, then we should expect recognition memory tests to engage working memory relatively more in apes than in monkeys. We evaluated this hypothesis by comparing the contributions of working memory and familiarity with recognition memory performance in orangutans and rhesus monkeys. Because the orangutans and monkeys here compared have different experience with cognitive testing, we aimed to compare the relative contributions of working memory and familiarity in each species, rather than the absolute accuracy of the two species in a particular memory test. This follows a logic similar to that used in many comparative anatomical studies; for example, those cited here that found the prefrontal cortex is larger in apes relative to body weight or visual cortex volume, rather than simply absolute volume.The relative contributions of working memory and familiarity to behavior can be measured in visual recognition memory tests. In these tests subjects study a sample image at the beginning of each trial and after a delay they are presented with a test consisting of the recently seen sample image among distractors (Fig. 1). The images used in these tests can either be repeated, such that the subject''s job is to determine which image in a set of familiar images was seen most recently, or the images can be trial unique, such that at test subjects need to discriminate a previously seen image from novel distractors. Working memory is critical for solving tests with repeating images, but much less so for tests using trial unique images, where familiarity plays a much greater role (Brady and Hampton 2018a). Monkeys (Jitsumori et al. 1988; Basile and Hampton 2013a) and apes (Harlow 1944; Hayes and Thompson 1953) are more accurate and better tolerate long delay intervals in tests with trial-unique stimuli, when familiarity can support performance. Experimentally naïve monkeys require comparatively little training to demonstrate proficient use of familiarity as a mnemonic cue, compared with the training required to become proficient in using working memory (Mishkin and Delacour 1975). Active working memory and passive familiarity are independent mnemonic processes that can be doubly dissociated. Working memory is impaired by a concurrent cognitive load imposed during the memory interval, while familiarity is not affected (Logie 1986; Jacoby et al. 1989; Basile and Hampton 2013a; Brady and Hampton 2018a). Completing the double dissociation, equating the familiarity of the sample and distractor images during study impairs choice based on familiarity, but not working memory (Brady and Hampton 2018a). Thus, recognition memory tests may allow us to compare the relative contributions of these two memory processes with recognition performance across species.Open in a separate windowFigure 1.Recognition memory tests with repeating and trial-unique images. (A) In tests with trial-unique images, each image was only used once as a sample or a distractor within a session. (B) When tested with repeating images, the images were the same on each trial. The sample image was pseudorandomly selected each trial such that each image appeared equally often as the sample or as a distractor.One might expect orangutans to show greater dependence on working memory compared with rhesus monkeys for at least two reasons. First, working memory is highly refined in humans and orangutans are more closely related to humans phylogenetically, sharing a common ancestor 13 million to 14 million years ago (Stewart and Disotell 1998), whereas rhesus monkeys and humans shared a common ancestor ∼32 million years ago (Roos and Zinner 2015). Second, orangutans have a relatively larger prefrontal cortex compared with monkeys (Rilling 2006; Passingham and Smaers 2014). We compared the ability of rhesus monkeys and orangutans to maintain images from different sets in working memory. We also determined the extent to which familiarity contributed to recognition memory performance. Across three experiments, we observed striking species differences. We found that in orangutans, recognition memory performance for both repeating and trial-unique images was controlled by working memory. In contrast, monkeys relied on working memory for repeating images, and on familiarity for trial-unique images. Furthermore, monkeys dramatically outperformed orangutans in tests that exceeded the capacity and duration of working memory, and thus depended on familiarity.     

Transfer of serial reversal learning in the pigeon

Pigeons were trained on a series of reversals of a simultaneous visual discrimination and were then shifted to a second series of reversals with different visual discriminanda. Pigeons that were given discrimination reversals with one pair of colours (Group Colour) and then shifted to a second pair of colours made fewer errors with the second pair than the first. In contrast, pigeons that were initially given reversals with a pair of orientations (Group Orientation) and then shifted to colours made as many errors during colour reversals as Group Colour had during initial colour training. When birds in Group Colour were subsequently shifted to orientation discrimination reversals, they performed no better than Group Orientation had during initial orientation training. The present results suggest that positive transfer from one series of discrimination reversals to a second, independent series may be constrained by the nature of the stimulus shift.     

Ontogenetic dissociation between habit learning and recognition memory in capuchin monkeys (Cebus apella)

The performance of young and adult capuchin monkeys (Cebus apella) on a Concurrent Discrimination Learning (CDL) test and a Delayed Non-Matching to Sample (DNMS) task were investigated. Results indicate that all subjects were able to learn the CDL test with 20-pairs simultaneously and retain this stimulus/reward association within 24-h interval. In contrast, young subjects did not perform the DNMS task with the same proficiency as adults. While adults' scores were above chance across all memory test delays, the young capuchin monkeys performed the test by chance level. These results support the hypothesis that these two tasks require different cognitive processes mediated by two independent neural systems with a differentiated ontogenetic development. Moreover, they provide evidence that this dissociation occurs not only in humans and Old World monkeys but also in the New World capuchin monkeys indicating that this species can be a valuable alternative model for investigations of the neurobiological basis of memory.     

Prospective memory in the formation of learning sets by rhesus monkeys (Macaca mulatta)

In conventional discrimination learning-set formation, it is possible that rhesus monkeys (Macaca mulatta) learn to lay down prospective memories by anticipating the next trial and deciding in advance what choice will be made. To test this hypothesis, the authors administered discrimination problems with 24-hr intertrial intervals, predicting that these long intervals would disrupt or prevent the putative anticipation of the next trial. Confirming their expectation, the authors found no indication of learning-set formation under these conditions.     

Individual differences in working memory capacity and learning: Evidence from the serial reaction time task

High and low working memory (WM) capacity individuals performed the serial reaction time task under both incidental and intentional learning conditions to determine the role of WM capacity in the learning of sequential information. WM capacity differences emerged in conditions of intentional but not incidental learning, indicating that individual differences in WM capacity occur in tasks requiring some form of control, with little difference appearing on tasks that required relatively automatic processing. Furthermore, an index of learning was significantly related to a measure of general fluid intelligence under intentional conditions only. Thus, the degree of learning was significantly related to higher order cognition, but only when intentional processing was emphasized.     

Hemispatial neglect and serial order in verbal working memory

Working memory refers to our ability to actively maintain and process a limited amount of information during a brief period of time. Often, not only the information itself but also its serial order is crucial for good task performance. It was recently proposed that serial order is grounded in spatial cognition. Here, we compared performance of a group of right hemisphere-damaged patients with hemispatial neglect to healthy controls in verbal working memory tasks. Participants memorized sequences of consonants at span level and had to judge whether a target consonant belonged to the memorized sequence (item task) or whether a pair of consonants were presented in the same order as in the memorized sequence (order task). In line with this idea that serial order is grounded in spatial cognition, we found that neglect patients made significantly more errors in the order task than in the item task compared to healthy controls. Furthermore, this deficit seemed functionally related to neglect severity and was more frequently observed following right posterior brain damage. Interestingly, this specific impairment for serial order in verbal working memory was not lateralized. We advance the hypotheses of a potential contribution to the deficit of serial order in neglect patients of either or both (1) reduced spatial working memory capacity that enables to keep track of the spatial codes that provide memorized items with a positional context, (2) a spatial compression of these codes in the intact representational space.     

Lexical learning in bilingual adults: the relative importance of short-term memory for serial order and phonological knowledge

Studies of monolingual speakers have shown a strong association between lexical learning and short-term memory (STM) capacity, especially STM for serial order information. At the same time, studies of bilingual speakers suggest that phonological knowledge is the main factor that drives lexical learning. This study tested these two hypotheses simultaneously in participants with variable levels of English-French bilingual proficiency. A word-nonword paired-associate learning task was administered, with nonwords obeying French phonotactic patterns. French phonological knowledge was estimated by a composite French proficiency score summarizing productive and receptive French vocabulary knowledge as well as quantitative and qualitative measures of French exposure. STM measures maximized retention of order information (serial order reconstruction) or retention of phonological item information (single nonword delayed repetition). The French proficiency score and the serial order STM measure independently predicted performance on the paired-associate learning task. These results highlight the conjoined role of phonological knowledge and serial order STM in lexical learning. Importantly, serial order STM remains a strong predictor of lexical learning, even for bilingual individuals who have broad phonological knowledge.     

Two types of serial dependence in visual working memory

Stimulus representations in working memory depend on memory traces of past stimuli both from previous trials and from the current trial. However, it is unclear whether the same or different mechanisms underlie this serial dependence across and within trials. We directly contrasted estimates of bias for pairs of immediately successive stimuli across and within trials. In each trial, participants memorized two consecutive motion direction stimuli (S1 and S2) and after a short delay were cued to report one of them. We found serial dependence across trials: The current S1 was attracted towards the preceding S2 when the latter had been cued for report. In contrast, within the same trial S2 was repulsed from S1. In addition, repulsion within a trial occurred for a broader range of motion direction differences between stimuli than attraction across trials. A second experiment in which 25% of trials did not require a response demonstrated that across‐trial attraction did not depend on whether the previous S2 actually had to be reported. Our findings provide evidence for two types of serial dependence operating across and within trials. They support the notion of different mechanisms integrating or segregating current from similar past memory contents depending on their task relevance.     

The effects of age and professional expertise on working memory performance

Differences in professional choice and experience may explain age differences in working memory performance of elderly people. The aim of this study was to examine whether expertise and prolonged practice in verbal and visuo‐spatial abilities reduce age differences in laboratory working memory tasks. The effects of age and expertise on working memory performance were examined in three age groups in two different experiments. Firstly, the role of visuo‐spatial expertise was analysed by examining age differences in architects. Secondly, people with extensive experience in verbal abilities (literary people) were tested in order to evaluate the effect of professional verbal experience. Architects and literary people outperformed a group of unselected age peers on tasks related to professional expertise only, but not on general working memory tests. There was no interaction between age and experience, suggesting that professional experience does not increase differences between experts and non experts and cannot modulate age‐related effects. Copyright © 2008 John Wiley & Sons, Ltd.     

Perceptual expertise enhances the resolution but not the number of representations in working memory

Despite its central role in cognition, capacity in visual working memory is restricted to about three or four items. Curby and Gauthier (2007) examined whether perceptual expertise can help to overcome this limit by enabling more efficient coding of visual information. In line with this, they observed higher capacity estimates for upright than for inverted faces, suggesting that perceptual expertise enhances visual working memory. In the present work, we examined whether the improved capacity estimates for upright faces indicates an increased number of "slots" in working memory, or improved resolution within the existing slots. Our results suggest that perceptual expertise enhances the resolution but not the number of representations that can be held in working memory. These results clarify the effects of perceptual expertise in working memory and support recent suggestions that number and resolution represent distinct facets of working memory ability.     

Discrimination of faces and houses by rhesus monkeys: the role of stimulus expertise and rotation angle

The face inversion effect, or impaired recognition of upside down compared to upright faces, is used as a marker for the configural processing of faces in primates. The inversion effect in humans and chimpanzees is strongest for categories of stimuli for which subjects have considerable expertise, primarily conspecifics’ faces. Moreover, discrimination performance decreases linearly as faces are incrementally rotated from upright to inverted. This suggests that rotated faces must be transformed, or normalized back into their most typical viewpoint before configural processing can ensue, and the greater the required normalization, the greater the likelihood of errors resulting. Previous studies in our lab have demonstrated a general face inversion effect in rhesus monkeys that was not influenced by expertise. Therefore, the present study examined the influence of rotation angle on the visual perception of face and nonface stimuli that varied in their level of expertise to further delineate the processes underlying the inversion effect in rhesus monkeys. Five subjects discriminated images in five orientation angles. Results showed significant linear impairments for all stimulus categories, including houses. However, compared to the upright images, only rhesus faces resulted in worse performance at rotation angles greater than 45°, suggesting stronger configural processing for stimuli for which subjects had the greatest expertise.     

Selective inactivation of adenosine A(2A) receptors in striatal neurons enhances working memory and reversal learning

The adenosine A(2A) receptor (A(2A)R) is highly enriched in the striatum where it is uniquely positioned to integrate dopaminergic, glutamatergic, and other signals to modulate cognition. Although previous studies support the hypothesis that A(2A)R inactivation can be pro-cognitive, analyses of A(2A)R's effects on cognitive functions have been restricted to a small subset of cognitive domains. Furthermore, the relative contribution of A(2A)Rs in distinct brain regions remains largely unknown. Here, we studied the regulation of multiple memory processes by brain region-specific populations of A(2A)Rs. Specifically, we evaluated the cognitive impacts of conditional A(2A)R deletion restricted to either the entire forebrain (i.e., cerebral cortex, hippocampus, and striatum, fb-A(2A)R KO) or to striatum alone (st-A(2A)R KO) in recognition memory, working memory, reference memory, and reversal learning. This comprehensive, comparative analysis showed for the first time that depletion of A(2A)R-dependent signaling in either the entire forebrain or striatum alone is associated with two specific phenotypes indicative of cognitive flexibility-enhanced working memory and enhanced reversal learning. These selective pro-cognitive phenotypes seemed largely attributed to inactivation of striatal A(2A)Rs as they were captured by A(2A)R deletion restricted to striatal neurons. Neither spatial reference memory acquisition nor spatial recognition memory were grossly affected, and no evidence for compensatory changes in striatal or cortical D(1), D(2), or A(1) receptor expression was found. This study provides the first direct demonstration that targeting striatal A(2A)Rs may be an effective, novel strategy to facilitate cognitive flexibility under normal and pathologic conditions.