Recognition and Pattern Separation in Aging

Our results are consistent with previous studies showing that younger and older adults did not differ on identifying old objects while older adults performed significantly worse compared to younger adults when identifying similar objects (Davidson et al., Reference Davidson, Vidjen, Trincao-Batra and Collin2019; Stark et al., Reference Stark, Yassa, Lacy and Stark2013; Stark et al., Reference Stark, Stevenson, Wu, Rutledge and Stark2015; Stark & Stark, Reference Stark and Stark2017; Toner et al., Reference Toner, Pirogovsky, Kirwan and Gilbert2009). We suggest that age-related impairments in pattern separation but not recognition occur because of inefficiencies in utilizing subtle perceptual details (Burke et al., Reference Burke, Gaynor, Barnes, Bauer, Bizon, Roberson and Ryan2018, Carr et al., Reference Carr, Castel and Knowlton2015; Kensinger & Schacter, Reference Kensinger and Schacter1999; Stark et al., Reference Stark, Yassa, Lacy and Stark2013; Stark & Stark, Reference Stark and Stark2017). During object recognition, participants may be able to rely on familiarity when recognizing a previously presented coffee mug. Utilizing perceptual details, however, is especially critical in differentiating between highly similar objects such as two similar coffee mugs (Yassa et al., Reference Yassa, Lacy, Stark, Albert, Gallagher and Stark2011).

Our results suggest that it is not simply that older adults perform poorly on pattern separation, but rather that they commit a specific kind of error that younger adults do not make. When older adults make errors, they are more likely to identify similar objects as old compared to younger adults, as reflected in our error difference score. Calculating a difference by subtracting the proportion of identifying similar objects as old from new can indicate if groups were biased to commit one error over another. This is additional evidence for an age-related decline in utilizing the details to orthogonalize representations in the brain for accurate memory retrieval. Similar findings that indicate older adults identify similar objects as old have been shown in other studies as well (Davidson et al., Reference Davidson, Vidjen, Trincao-Batra and Collin2019; Pidgeon & Morcom, Reference Pidgeon and Morcom2014; Stark et al., Reference Stark, Yassa, Lacy and Stark2013; Stark et al., Reference Stark, Stevenson, Wu, Rutledge and Stark2015). These errors suggest that older adults could be using a holistic representation when making similarity judgements. Yassa and Stark (Reference Yassa and Stark2011) suggest that aging is associated with a shift from pattern separation toward pattern completion, likely related to functional and structural changes in the MTL (Yassa & Stark, Reference Yassa and Stark2011). Younger adults, on the other hand, may have a slight bias to identify similar objects as new, particularly on white backgrounds. However, they showed less bias in general, with error difference scores close to zero across all contexts.

The Impact of Context on Recognition and Pattern Separation

For recognition memory, old objects on a repeated white background and on a repeated scene resulted in better memory scores than shifting the context to a novel scene. Both groups experienced an equivalent decrease in recognition memory performance when an old object was placed on a novel scene that was never seen before. This replicated previous findings from our lab showing that reinstating the context at retrieval for object recognition benefited older and younger adults in the same way (Memel & Ryan, Reference Memel and Ryan2017). It is important to note that repeating a white background had the same benefit as repeating a complex visual scene. Objects and contexts are hypothesized to be processed holistically and automatically rather than two separate components, making recognition of the object more difficult when it is shifted to a novel scene (Hasher & Zacks, Reference Hasher and Zacks1979; Hayes et al., Reference Hayes, Nadel and Ryan2007). Keeping contexts consistent between encoding and retrieval have shown benefits for recognition memory for objects (Gutchess et al., Reference Gutchess, Hebrank, Sutton, Leshikar, Chee, Tan, Goh and Park2007; Hayes et al., Reference Hayes, Glisky, McAllister, Greenleaf, Ketcham, Nadel and Ryan2005; Hayes et al., Reference Hayes, Nadel and Ryan2007; Memel & Ryan, Reference Memel and Ryan2017; Racsmány et al., Reference Racsmány, Bencze, Pajkossy, Szőllősi and Marián2021), words (Craik & Schloerscheidt, Reference Craik and Schloerscheidt2011), and faces (Hayes et al., Reference Hayes, Baena, Truong and Cabeza2010). These benefits are true for tasks that use semantically related scenes (Hayes et al., Reference Hayes, Nadel and Ryan2007) and for tasks that superimpose objects on irrelevant backgrounds (Racsmány et al., Reference Racsmány, Bencze, Pajkossy, Szőllősi and Marián2021). Unlike the experiments described in Hayes et al. (Reference Hayes, Nadel and Ryan2007), objects in this task were not embedded naturalistically as objects from this task were superimposed on backgrounds. Racsmány et al. (Reference Racsmány, Bencze, Pajkossy, Szőllősi and Marián2021) also superimposed objects; however, these scenes were not semantically related to the object. For example, a picture of a bird cage was superimposed in a bathroom. The impact of context shift therefore appears to be robust, irrespective if objects are embedded naturalistically or superimposed.

In contrast to object recognition, context impacted pattern separation for older and younger adults differently. All participants had more difficulty identifying similar objects when they were placed in a scene, repeated or novel, compared to a repeated white background. The white background and the repeated scene impacted recognition of old objects in the same way, whereas the repeated scene impaired recognition for similar objects. Although the white background is still a repeated context, the repeated scenes have more familiar components than a white background, potentially leading participants to incorrectly identify similar objects as old. Additionally, repeated scenes increased the Similarity False Alarms for all participants, thus having the largest impact on the corrected pattern separation scores in the Repeated Scene context condition. Interestingly, a post hoc analysis of the uncorrected pattern separation scores showed that performance in the Repeated Scene and Repeated White contexts were not statistically different, t(111) = 1.14, ns.

Surprisingly, identifying similar objects in novel or repeated scenes did not differ. We hypothesized that performance in novel scenes would be better than repeated scenes because novel scenes do not have any familiar components other than any potential familiarity produced from the similar object itself. The novel scenes in this study are still semantically related to the similar object. For example, in Figure 1, a bar of soap is presented in a laundromat and then another similar bar of soap is presented in a bathroom. One explanation could be that the relationship between the soap and the new background led participants to be less accurate when identifying the similar object on novel, but related scenes (Bar & Ullman, Reference Bar and Ullman1996). Bar (Reference Bar2004) proposed that visual information, such as a scene, can be quickly extracted to activate “context frames,” which would include objects typically associated with that scene. The activation of semantically related objects could have overshadowed the subtle details of the similar object on the screen, leading to identifying a similar object as old. Initially it may appear as if the repeated scene and novel scene have the same impact on pattern separation, given they both resulted in poorer performance than the repeated white background. However, a deeper look at the Similarity False Alarms would suggest that these scene conditions are indeed impacting pattern separation differently. Unlike the repeated scene, novel scene did not lead participants to commit many Similarity False Alarms. When Similarity False Alarms were not corrected for, the scores within the repeated scenes become significantly higher than the scores in the novel scenes. Without correcting for Similarity False Alarms, it may look as if repeated scenes resulted in better accuracy for similar objects compared to novel scenes. However, the elevated Similarity False Alarms would suggest that the repeated scene led to a general tendency to call objects similar, increasing both their accuracy score in addition to their Similarity False Alarms. Neither the repetition of the white background nor the novel scene resulted in the same elevation of Similarity False Alarms, suggesting a unique effect from the repeated scene on Similarity False Alarms.

Age-related declines in the ability to inhibit irrelevant information could be another explanation for the context effects we observed among older adults (for a recent review, see Amer et al., Reference Amer, Wynn and Hasher2022). By this view, poorer inhibitory control among older adults may result in goal-irrelevant information being incorporated into the memory representation to a greater degree than younger adults, and this information may then interfere with successful retrieval. For example, in studies by Hasher and colleagues (Campbell et al., Reference Campbell, Hasher and Thomas2010; Campbell & Hasher, Reference Campbell and Hasher2018), participants were shown pictures with superimposed irrelevant words in a 1-back working memory task. A surprise paired associate memory task followed, where picture-word pairs were either preserved or rearranged from the initial encoding phase. Older adults performed better when the picture-word pair was preserved relative to rearranged pairs or words presented on a novel picture (Biss et al., Reference Biss, Campbell and Hasher2013). Younger adults, on the other hand, did not show any differences in performance between the type of pairs, suggesting that older, but not younger adults, integrated the visual context into their memory representation, which benefitted memory performance.

An age-related difference in the ability to inhibit contextual information could explain the heighted context effect observed among older adults in the present study. However, our results, as well as prior studies of object recognition (Hayes et al., Reference Hayes, Glisky, McAllister, Greenleaf, Ketcham, Nadel and Ryan2005; Hayes et al., Reference Hayes, Nadel and Ryan2007), demonstrated that younger adults are also highly influenced by context. In a series of object recognition studies with young adults, Hayes et al. (Reference Hayes, Nadel and Ryan2007) demonstrated that changing the visual context always resulted in impaired object recognition, even when participants were explicitly told to disregard the background. In the present study, objects presented on a novel scene resulted in poorer recognition performance for both younger and older adults compared to objects presented on either a repeated scene or a repeated white background. Furthermore, both younger and older adults were more accurate in identifying similar objects when they were presented on repeated white backgrounds. Taken together, these results are consistent with the notion that binding objects and the surrounding context within a scene is obligatory and automatic, and that all components of the representation are utilized when making memory judgements. The results in the present study suggest that the integration of visual context to the representation may be age-invariant. The results may be better explained by differences in the reliance on context among older and younger adults during memory retrieval, rather than a decline in inhibitory control.

Detailed and Holistic Information in Aging

By presenting similar objects across stable and shifting contexts, our study evaluated how detailed and holistic contextual information is differentially utilized by younger and older adults during pattern separation. Older adults had more difficulty identifying similar objects and, importantly, misidentified similar objects as old across all contexts compared to younger adults. The results fit well with the hypothesis that older adults overemphasize holistic information and underutilize details when assessing memory for objects (Burke et al., Reference Burke, Gaynor, Barnes, Bauer, Bizon, Roberson and Ryan2018; Gutchess et al., Reference Gutchess, Hebrank, Sutton, Leshikar, Chee, Tan, Goh and Park2007). Older adults have more difficulty using the details to distinguish between highly similar objects (Camfield et al., Reference Camfield, Fontana, Wesnes, Mills and Croft2018; Davidson et al., Reference Davidson, Vidjen, Trincao-Batra and Collin2019; Pidgeon & Morcom, Reference Pidgeon and Morcom2014; Reagh et al., Reference Reagh, Ho, Leal, Noche, Chun, Murray and Yassa2016; Stark et al., Reference Stark, Yassa, Lacy and Stark2013; Stark et al., Reference Stark, Stevenson, Wu, Rutledge and Stark2015; Stark & Stark, Reference Stark and Stark2017; Toner et al., Reference Toner, Pirogovsky, Kirwan and Gilbert2009), and require a greater degree of dissimilarity between features in order to effectively discriminate between items (Wilson et al., Reference Wilson, Gallagher, Eichenbaum and Tanila2006; Yassa et al., Reference Yassa, Lacy, Stark, Albert, Gallagher and Stark2011). Additionally, older adults showed an overreliance on the context. Repeating the scene increased the likelihood that older adults identified similar objects as old objects, and this increase was not seen in younger adults.

The overreliance on holistic information observed among older adults is consistent with the changes in MTL circuitry that are observed during normal aging (Burke et al., Reference Burke, Gaynor, Barnes, Bauer, Bizon, Roberson and Ryan2018; Wilson et al., Reference Wilson, Gallagher, Eichenbaum and Tanila2006; Yassa et al., Reference Yassa, Lacy, Stark, Albert, Gallagher and Stark2011; Yassa & Stark, Reference Yassa and Stark2011). Yassa and Stark (Reference Yassa and Stark2011) suggest that the loss of inhibitory inputs to the dentate gyrus/CA3 region of the hippocampus result in a shift away from pattern separation and toward pattern completion, where incomplete information may be sufficient to access previously stored representations (Marr, Reference Marr1971; Yassa & Stark, Reference Yassa and Stark2011). This shift would account for older adults’ overall propensity to identify similar objects as old, across all context conditions. Although Yassa et al. (Reference Yassa, Lacy, Stark, Albert, Gallagher and Stark2011) did not evaluate the impact of context on pattern separation, their hypothesis may also account for a broader shift toward pattern completion where a repeated scene further exacerbates this error.

A recent model of age-related changes to MTL circuity posits two distinct networks between the hippocampus, PRC, and parahippocampal cortex (PHC) (Burke et al., Reference Burke, Gaynor, Barnes, Bauer, Bizon, Roberson and Ryan2018). In contrast to the PRC and PHC carrying non-spatial and spatial information, respectively (Barense et al., Reference Barense, Henson, Lee and Graham2010; Mormann et al., Reference Mormann, Simon, Cerf, Ison, Kraskov, Tran, Knieling, Quiroga, Koch and Fried2017), more recent evidence from animal studies suggests that these networks are not content driven. Rather, two parallel, computationally distinct pathways carry detailed and holistic information that incorporates both spatial and non-spatial information (see Figure 5). One pathway involves direct projections, carrying detailed information, from PRC and PHC to CA1. A second pathway involves indirect projections, carrying holistic information, from PRC and PHC via entorhinal cortex, projecting to CA3. Age-related damage to PRC results in loss of integrity to the direct pathway, as well as a normal inhibition to the indirect pathway. The net effect is a shift away from perceptual and spatial detail, and a greater reliance on holistic processing. Our results are consistent with this shift, as older adults were impaired in utilizing subtle, perceptual details to distinguish between old and similar objects and were influenced to a greater degree by holistic information provided by both the similar objects and the repeated scenes.

Figure 5.

This is adapted from Burke et al. (Reference Burke, Gaynor, Barnes, Bauer, Bizon, Roberson and Ryan2018), Figure 2. Two parallel pathways from the PRC and PHC carry direct and indirect projections into the hippocampus. The direct pathway carries detailed information and the indirect pathway carries holistic information (referred to as “gist” or course network in Burke et al., Reference Burke, Gaynor, Barnes, Bauer, Bizon, Roberson and Ryan2018). In aging, decreased PRC activation leads to less excitation of the direct pathway and less inhibition in the indirect pathway, resulting in a greater emphasis on holistic information.

A Subtle Effect of ϵ4

Finally, ϵ4 did not have a significant impact on most outcomes. However, analysis of Similarity False Alarms revealed a triple interaction between ϵ4, context, and age. In the repeated scene, younger ϵ4 carriers had fewer Similarity False Alarms compared to younger noncarriers. The subtle advantage for younger ϵ4 carriers suggests that they were less influenced by the repeated scene. This pattern flipped among older adults, such that older ϵ4 carriers made more Similarity False Alarms compared to noncarriers, suggesting that they were influenced to a greater degree by the repeated scene. We originally hypothesized that older ϵ4 carriers would be less biased by repeated scenes, potentially due to elevated neuropathology in the PRC. However, this finding suggests a greater bias from the repeated scenes. One possibility is that preclinical pathology associated with ϵ4 results in additional damage to the indirect pathway, which appears to produce greater bias toward holistic information, rather than less, compared to noncarriers. If early neuropathology is responsible for these subtle changes among older ϵ4 carriers, then performance on tasks other than pattern separation would also likely be affected. For example, object discrimination, which does not depend on memory and requires discrimination of stimuli with overlapping features, is well-documented to rely the PRC (Barense et al., Reference Barense, Gaffan and Graham2007; Barense et al., Reference Barense, Henson, Lee and Graham2010; Ryan et al., Reference Ryan, Cardoza, Barense, Kawa, Wallentin‐Flores, Arnold and Alexander2012). To our knowledge, no study exists currently that has evaluated the relationship between object discrimination and pattern separation. Based on our model, one would expect that these two distinct tasks would be correlated, at least among older adults and potentially even more strongly among individuals who are at high risk for developing AD. The effect of ϵ4 is novel, and clearly warrants replication and further study. It is important to note, however, that ϵ4 cannot be considered a proxy for neuropathology. More direct quantification of tauopathy would be needed to understand these relationships. Finally, the number ϵ4 carriers, particularly in the young, may have also limited our power to see other main effects or interactions with ϵ4.

The ϵ4 interaction may support the antagonistic pleiotropy hypothesis (Han & Bondi, Reference Han and Bondi2008; Tuminello & Han, Reference Tuminello and Han2011). Antagonistic pleiotropy describes a gene that has beneficial effects on fitness early in life, and detrimental effects later in life (Albin, Reference Albin1993; Williams, Reference Williams1957). A review from Tuminello and Han (Reference Tuminello and Han2011), described how some studies found cognitive benefits among young ϵ4 carriers compared to noncarriers (Bloss et al., Reference Bloss, Delis, Salmon and Bondi2010; Marchant et al., Reference Marchant, King, Tabet and Rusted2010; Rusted et al., Reference Rusted, Evans, King, Dowell, Tabet and Tofts2013; Mondadori et al., Reference Mondadori, de Quervain, Buchmann, Mustovic, Wollmer, Schmidt, Boesiger, Hock, Nitsch, Papassotiropoulos and Henke2007). However, some studies do not show ϵ4 advantages in younger adults (Dennis et al., Reference Dennis, Browndyke, Stokes, Need, Burke, Welsh-Bohmer and Cabeza2010; Filbey et al., Reference Filbey, Slack, Sunderland and Cohen2006; Ruiz et al., Reference Ruiz, Castillo, Labayen, Moreno, Fuentes, Lamuno, Granda, Lucia and Ortega2010; Evans et al., Reference Evans, Dowell, Tabet, King, Hutton and Rusted2017; Filippini et al., Reference Filippini, MacIntosh, Hough, Goodwin, Frisoni, Smith, Matthews, Beckmann and Mackay2009; Ihle et al., Reference Ihle, Bunce and Kliegel2012; Weissberger et al., Reference Weissberger, Nation, Nguyen, Bondi and Han2018). Meta-analyses of younger ϵ4 carriers and noncarriers indicate that variability in results are likely a due to a wide range of variables including tests used, ages included, control for other AD risk factors, and inclusion of ϵ2 carriers (Ihle et al., Reference Ihle, Bunce and Kliegel2012; Tuminello & Han, Reference Tuminello and Han2011; Weissberger et al., Reference Weissberger, Nation, Nguyen, Bondi and Han2018).

The impact of context on recognition memory was different compared to pattern separation. In recognition, context impacts older and younger adults in the same way, but differences in age emerged during pattern separation. Older adults were not able to utilize the perceptual details in order to distinguish between similar objects and relied more on holistic information, leading to a particular pattern of errors that younger adults did not make. Nonpathological ϵ4 aging may also perpetuate older adults’ greater sensitivity to holistic information.