Effect of aging differs for memory of object identity and object position within a spatial context

There has been considerable focus on investigating age-related memory changes in cognitively healthy older adults, in the absence of neurodegenerative disorders. Previous studies have reported age-related domain-specific changes in older adults, showing increased difficulty encoding and processing object information but minimal to no impairment in processing spatial information compared with younger adults. However, few of these studies have examined age-related changes in the encoding of concurrently presented object and spatial stimuli, specifically the integration of both spatial and nonspatial (object) information. To more closely resemble real-life memory encoding and the integration of both spatial and nonspatial information, the current study developed a new experimental paradigm with novel environments that allowed for the placement of different objects in different positions within the environment. The results show that older adults have decreased performance in recognizing changes of the object position within the spatial context but no significant differences in recognizing changes in the identity of the object within the spatial context compared with younger adults. These findings suggest there may be potential age-related differences in the mechanisms underlying the representations of complex environments and furthermore, the integration of spatial and nonspatial information may be differentially processed relative to independent and isolated representations of object and spatial information.

Advancing age is associated with changes in a number of cognitive domains (Erickson and Barnes 2003; Salthouse 2004; Craik and Bialystok 2006). Particularly age-related changes in episodic memory function have been frequently reported (Grady and Craik 2000; Craik and Bialystok 2006). In addition to a general decline in long-term retention, older adults show a reduced ability to differentiate between highly similar object representations (Yassa et al. 2011; Stark et al. 2013, 2015; Reagh et al. 2016; Berron et al. 2018) and object features (Yeung et al. 2017) compared with young adults. In contrast, spatial representations appear to be relatively spared (Fidalgo et al. 2016; Stark and Stark 2017) with older adults showing performance similar to young adults recognizing subtle changes in a spatial environment (Berron et al. 2018) and changes in the location of an object when presented on a blank screen (Reagh et al. 2016, 2018).The dissociation and integration of object and spatial information has been a key question in memory research. Older adults show significant impairments in memory binding and maintaining associations despite having intact memory for the individual items (Chalfonte and Johnson 1996; Naveh-Benjamin 2000; Old and Naveh-Benjamin 2008). This is also observed in object-location binding with impairments in recalling the specific location of objects (Kessels et al. 2007; Berger-Mandelbaum and Magen 2019; Muffato et al. 2019) as well as recalling the identity of an object within an environment (Schiavetto et al. 2002; Kessels et al. 2007; Mazurek et al. 2015). The binding of object-location information has been hypothesized to involve the medial temporal lobes, including the hippocampus (Postma et al. 2008), although age-related changes in the prefrontal cortex, posterior neocortex and other regions have also been implicated in object location and object identity tasks (Schiavetto et al. 2002; Meulenbroek et al. 2010). In the medial temporal lobes, the integration of object and spatial information is thought to arise from two parallel information processing streams (Eichenbaum 1999; Eichenbaum et al. 1999; Davachi 2006; Ranganath and Ritchey 2012; Knierim et al. 2013). One pathway, commonly referred to as the “what” pathway involves the perirhinal cortex and the lateral entorhinal cortex, and is thought to predominately process information about objects, items and events, while the “where” pathway involving the parahippocampal cortex and the medial entorhinal cortex is thought to process contextual and spatial information. Information from both pathways is projected to the hippocampus, which is then thought to integrate the spatial and nonspatial information into a cohesive “memory space” through a mechanism that is common to both object or episodic and spatial information (Eichenbaum et al. 1999).However, emerging evidence suggests the processing of object and spatial information may be more integrated than previously thought with the lateral entorhinal cortex processing multimodal information, receiving both object and spatial information (Witter et al. 2017; Doan et al. 2019; Nilssen et al. 2019). In rodent studies, the lateral entorhinal cortex has been reported to be involved in the encoding of features from both the object and the environment (Deshmukh and Knierim 2011; Yoganarasimha et al. 2011; Deshmukh et al. 2012; Knierim et al. 2013). Rodent studies using single cell recordings in the lateral entorhinal cortex show that neurons in this region encode object-related information as well as spatial information about the object (e.g., position in relationship to the environment). These studies also show cells in the lateral entorhinal cortex that track the position of an object in the environment and do not fire when that object is no longer present (Deshmukh and Knierim 2011). A different subset of cells (“object trace cells”) have been reported to fire in previously experienced positions of an object within an environment (Deshmukh and Knierim 2011; Tsao et al. 2013). Lateral entorhinal cortex lesioned rodents show no impairment in performing an object-recognition task, but are impaired at recognizing spatial changes and object changes within a set of objects in an environment including position changes of the objects (Van Cauter et al. 2013) and previously learned object-place and object-context associations (Wilson et al. 2013a; Chao et al. 2016). Together, these findings suggest that, beyond encoding information about objects, the lateral entorhinal cortex encodes contextual information and may be binding nonspatial and spatial information, specifically encoding information about objects and certain spatial properties, including information about the object''s position within environment.Few studies have examined the role of the lateral entorhinal cortex in encoding object identity, object position or changes to the spatial context in humans. Reagh and Yassa (2014) report that subtle perceptual differences between similar objects (e.g., two slightly different apples) elicits activity observed with functional magnetic resonance imaging (fMRI) in both the lateral entorhinal cortex and perirhinal cortex, while changes to an object''s position on a blank screen elicited activity in both the parahippocampal cortex and medial entorhinal cortex. Subsequent studies in older adults show impaired performance recalling the identity of object (Reagh and Yassa 2014; Stark and Stark 2017; Yeung et al. 2017; Berron et al. 2018; Reagh et al. 2018) but similar performance recalling position of the object on a screen compared with young adults (Reagh et al. 2016, 2018). However, these studies examined memory for object identity and object position on a blank screen, devoid of any spatial or contextual information. Given the findings from rodent studies, it appears that object identity and object position information are represented in relationship to the spatial environment in which they occur.To examine the integration of nonspatial and spatial information, novel stimuli were developed to mimic real-life environments where objects could occur within the environment, more closely resembling animal studies in which rodents experience objects within an environment. A series of scenes were designed to have the same perspective, spatial dimensions and outdoor scenery (Fig. 1A). Scenes were classified into five general categories: living room, dining room, kitchen, bedroom, and office rooms to allow for the placement of categorically congruent furniture (Fig. 1B). Critically, within each scene, two to five different positions were defined that an object could logically occupy (Fig. 1C). The scene stimuli were first validated using mnemonic ratings and subsequently used in a novel object-in-context task to assess memory for object identity and object position in context and examine age-related changes in performance on this task in cognitively normal older adults compared with young adults.Open in a separate windowFigure 1.Task stimuli. (A) Scenes were designed to have identical dimensions and a similar perspective. (B) Scenes were designed to have two to five different positions where an object could be reasonably placed. Across all scenes, the same general positions were available for object placement. (C) Example of a scene with an object as seen by the participant. No object was present in the scenes for the stimulus validation study.