Visual object pattern separation deficits in nondemented older adults

Abstract

Young and nondemented older adults were tested on a continuous recognition memory task requiring visual pattern separation. During the task, some objects were repeated across trials and some objects, referred to as lures, were presented that were similar to previously presented objects. The lures resulted in increased interference and an increased need for pattern separation. For each object, the participant was asked to indicate whether (1) this was the first time the object was seen (new), (2) the object was seen previously (old), or (3) the object was similar to a previous object (similar). Older adults were able to correctly identify objects as old or new as well as young adults; however, older adults were impaired when identifying lures as similar. Therefore, pattern separation may be less efficient in older adults resulting in poorer recognition memory performance when interference is increased.A primary region of the brain affected by normal aging is the hippocampus in humans (Good et al. 2001;Allen et al. 2005;Driscoll and Sutherland 2005;Raz et al. 2005;Walhovd et al. 2005) and animal models (Rosenzweig and Barnes 2003;Driscoll et al. 2006). However, the subregions of the hippocampus may be differentially affected by normal aging (Small et al. 2002(Small et al. , 2004. The dentate gyrus (DG) subregion may be particularly susceptible to age-related changes in both humans (Small et al. 2002) and animal models (Small et al. 2004;Patrylo and Williamson 2007), whereas aging may have less of an impact on pyramidal cells in the CA subregions (Small et al. 2002(Small et al. , 2004. In contrast, the CA subregions of the hippocampus may be more vulnerable to pathological aging associated with Alzheimer's disease (Braak and Braak 1996;Price et al. 2001;West et al. 2001). Therefore, tasks sensitive to dysfunction in particular subregions of the hippocampus may help to differentiate cognitive impairment associated with normal aging from pathological changes associated with Alzheimer's disease. Although hippocampal-dependent tasks are highly sensitive to age-related changes in the brain (for review, see Rosenzweig and Barnes 2003), behavioral studies in humans have not examined the performance of nondemented older adults on tasks shown to be particularly sensitive to DG function. As described in detail below, a key function of the DG may be to support pattern separation. Age-related changes in the DG may impair the ability to reduce similarity among new input patterns, resulting in decreased pattern separation (Wilson et al. 2006). Therefore, decreased efficiency in pattern separation may be a critical, but relatively unexamined, processing deficit in nondemented older humans.Pattern separation is described as a mechanism for separating partially overlapping patterns of activation so that one pattern may be retrieved as separate from other patterns (Gilbert et al. 2001;Gilbert and Kesner 2006;Kirwan and Stark 2007). The operation of a pattern separation mechanism is critical for reducing potential interference among ...

Cortical pattern separation and item-specific memory encoding

“…This may also be why responses here but not in the previous study were also less accurate for lures than for studied and novel items. The pattern observed here is consistent with previous findings of reduced performance for lures (e.g., Stark et al, 2013;Toner et al, 2009), and with claims that lure discrimination places greater demands on pattern separation (Kirwan and Stark, 2007; and/or post-retrieval processing (Brainerd et al, 2003;Morcom, 2015) and is therefore associated with reduced accuracy.…”

“…Faster RTs at study to both repeated and similar items are consistent with priming of similar items based on overlapping perceptual or conceptual features (Stenberg et al, 2009). Performance on the 'same/similar/new' recognition test was similar to that in previous reports (Garoff et al, 2005;Stark et al, 2013;Toner et al, 2009) with participants most often correctly classifying studied, lure and novel images as 'same', 'similar' and 'new', respectively.…”

Age-related memory deficits linked to circuit-specific disruptions in the hippocampus

“…Critically, the extent of this representational rigidity predicted the performance of older adults on an explicit recognition task that directly tested their pattern separation abilities. This task was used to demonstrate agerelated impairments in pattern separation (20,21). Further, there was evidence for a relationship between the rigidity in DG/CA3 fMRI activity and a simple standardized test of delayed recall performance, a memory measure that is known to be sensitive to hippocampal damage (44,45).…”

“…Converging evidence from animals (1) and humans (20,21,36) demonstrates that, on a behavioral level, pattern separation abilities are reduced with aging. This deficit is hypothesized to underlie We found a negative relationship between the left DG/CA3 slope of activity in older adults and their separation bias on an explicit recognition task designed to tax their pattern separation abilities, suggesting that processing in this region plays a key role in discrimination and that its dysfunction with age may underlie mnemonic deficits.…”

“…We (20) as well as others (21) have tested this hypothesis more explicitly in older adults by using an object discrimination task. Consistent with the predictions from the rodent work, both studies found that older adults tended to be biased more toward completion at the expense of separation.…”