Age effects on the neural processing of object-context associations in briefly flashed natural scenes
Introduction
Within very short exposure times such as a few tenths of ms, human observers are able to accurately recognize various objects in a visual complex scene (Biederman et al., 1974; Fei-Fei et al., 2007; Greene and Oliva, 2009; Thorpe et al., 1996). This impressive ability seems to strongly rely on the use of visual expectations based on our lifelong experience of the surrounding world (Bar and Ullman, 1996; Greene et al., 2015), thus facilitating perception on a daily basis. As a consequence, when scenes deviate from these expectations, i.e. when an object appears in a semantically incongruent environment, a deficit in fast object recognition performance is consistently observed (Biederman et al., 1982; Davenport and Potter, 2004; Joubert et al., 2008; Mudrik et al., 2010). Longer scene exposure times are needed to reliably report incongruent elements (Greene et al., 2015). We have previously shown that this difficulty in identifying incongruent objects in briefly-presented scenes is increased in older relative to younger adults, whereas rapid processing of congruent objects remains accurate until very old age (Rémy et al., 2013). Imaging results during passive viewing of natural scenes have suggested that older adults’ processing of background context is preserved, whereas processing of salient objects is diminished (Chee et al., 2006; Goh et al., 2007; Gutchess et al., 2006). Hence the dominant role of gist processing in fast scene perception, as reported in young adults (Greene et al., 2015; Mack et al., 2017), may possibly be emphasized in old age. To our knowledge, age-related differences in the neural substrates of fast visual processing of objects in natural scenes have not been investigated yet. The objective of the present functional magnetic resonance imaging (fMRI) study was to determine, in young and older adults, the neural structures involved in rapid categorization of objects presented in either congruent or incongruent contexts. In daily life, the ability to detect rapidly and accurately novel or unexpected objects appearing in our visual environment is critical, as a fast appropriate response may be needed. How aging affects this ability, and which aspects of fast visual scene processing undergo age-related changes, are therefore important questions to address.
When presented with brief natural scenes, participants can rapidly categorize either scene context (Fabre-Thorpe et al., 2001; Greene and Oliva, 2009; Joubert et al., 2009; Rousselet et al., 2005) or salient objects (Fize et al., 2011; Thorpe et al., 1996). If the natural scene includes congruent objects (a polar bear on the floe), strongly interconnected cortical representations, i.e. schemata or context frames (Bar, 2004; Biederman et al., 1982; Van Kesteren et al., 2012), activate, thus facilitating object identification. Conversely, incongruent scenes (a polar bear in a living room) may activate representations along the ventral stream that have not been repeatedly co-activated through lifelong experience of the surrounding environment. From brief exposure to congruent or incongruent scenes, object and context are processed in parallel along the ventral pathway, and there is evidence that both processing streams interfere early, at perceptual stages (Brandman and Peelen, 2017; Fabre-Thorpe, 2011; Mullin and Steeves, 2011). It has been proposed that perceiving incongruent object-context associations activates conflictual representations in high-level regions of the ventral pathway. The parahippocampal cortex (PHC), including the parahippocampal place area (PPA) in its posterior part, and the fusiform gyrus, which is part of the Lateral Occipital Complex (LOC), are candidate loci where this conflictual processing occurs. Indeed these regions have been involved in object-object or object-context relational processing (Goh et al., 2004; Gronau et al., 2008; Howard et al., 2011; Kim and Biederman, 2011). In particular, the PHC has been proposed to mediate representations for the familiar associations inherent to natural scenes (Aminoff and Tarr, 2015). In a previous fMRI study, increased PHC activity was found in response to incongruent vs. congruent object-context relationships in a group of young adults (Rémy et al., 2014), and the increase in the anterior part of the PHC was related with the increase in reaction times due to incongruence on a fast object categorization task. This suggests that exposure to previously-unexperienced contextual associations induced additional processing in the PHC that may have contributed to increase the time needed for object processing.
Fast processing of natural scenes and objects is robust with aging. Despite low-level visual deficits, such as reduced acuity, contrast sensitivity or color vision (Owsley, 2011), the ability to rapidly categorize isolated objects or contexts without any salient objects using short exposure times seems well preserved with age (Agnew and Pilz, 2017; Boucart et al., 2008; Lenoble et al., 2013; Lenoble et al., 2014; Ramanoël et al., 2015). This indicates that mechanisms involved in rapid gist recognition stay preserved in older adults, although processing of objects embedded in contexts remains challenging when scenes are briefly presented (Rémy et al., 2013). Using longer exposure times to natural stimuli that allow for ocular exploration, age-related differences in activity have been consistently demonstrated in high-level regions of the ventral pathway. Functional MRI studies have shown that neural response in ventral regions is less selective to specific categories of stimuli (Burianová et al., 2013; Carp et al., 2011; Goh et al., 2010; Park et al., 2004, 2012). A few studies have explored processing of objects embedded in contexts using either passive viewing or incidental encoding tasks (Chee et al., 2006; Goh et al., 2007; Gutchess et al., 2006; Jenkins et al., 2010). Using fMR-Adaptation experiments, neural adaptation in the PPA was found similar in older and young participants, suggesting preserved context processing with age. However, adaptation to repeated objects and to repeated object-context associations was decreased in the LOC and in the anterior PHC respectively for older participants, suggesting impaired object processing. It has been proposed that concurrent visual processing of both object and context is deficient with age due to reduced resources (Chee et al., 2006). Importantly, neural adaptation in the LOC was subject to cultural biases driven by lifelong experience within a given environment, as well as attentional biases related to task instructions, suggesting that scene ocular exploration contributes to these age-related effects. In agreement, natural viewing behavior in older adults was reported to be less driven by stimulus features than by explorative strategies (Açik et al., 2010). Greater influence of explorative strategies with age is consistent with increased frontal recruitment during processing of natural scenes (Burianová et al., 2013; Grady et al., 1994; Gutchess et al., 2005; Park et al., 2003) and motion stimuli (Biehl et al., 2017), in accordance with a Posterior- Anterior Shift with Aging (PASA) model (Davis et al., 2008). However it remains unclear whether a rapid visual task using flashed scenes, which does not permit visual exploration, will induce such age-related differences in ventral and frontal activity.
In the present fMRI study, behavioral performance and brain activity were compared between young and older adults completing a rapid object categorization task with briefly-presented scenes (100 ms). Such short exposure to stimuli prevented eye movements, while allowing for nearly maximal BOLD response in occipito-temporal regions (Grill-Spector et al., 2001). Objects were either non-domestic animals or pieces of furniture embedded in either natural outdoor or man-made indoor contexts, resulting in congruent or incongruent scenes. We first aimed at reproducing the behavioral result of a previous study showing a greater impairment in older participants when categorizing an object in an incongruent context, relative to young participants (Rémy et al., 2013). The main aim was to compare average levels and multivariate patterns of brain activity in response to congruent and incongruent scenes in both groups. We hypothesized that differences in activity in high-level regions of the ventral pathway possibly underlie the age-related impairment in fast incongruent object categorization. In particular, PPA activity may stay preserved with age, whereas LOC activity may be altered (Chee et al., 2006; Goh et al., 2007). We also hypothesized increased frontal activity in the older group during fast object categorization, possibly to compensate for altered object processing (Burianová et al., 2013; Gutchess et al., 2005). This increased frontal recruitment may be more pronounced in response to incongruent scenes, due to greater task difficulty.
Section snippets
Participants
Forty-eight healthy volunteers from two age groups were recruited for the study. Young participants (n = 22, 2 left-handed) were between 19 and 27 years old, and older participants (n = 26, 2 left-handed) were between 59 and 77 years old. Three participants were subsequently excluded: two older participants due to neurological abnormalities and one young participant due to excessive movement in the scanner. Information on the remaining 45 participants is given in Table 1. The study was approved
Behavioral results
Group results for accuracy and RT on the categorization task are shown on Fig. 2. Global accuracy varied from 85.7% to 99% in the young group, and from 81.5% to 98.8% in the older group. Young and older participants’ accuracies were equivalent (F (1,43) = 1.38, p = 0.25). Also accuracy was decreased in the incongruent relative to congruent condition (F (1,43) = 40.95, p < 10−7). This decrease related to incongruence was more pronounced in the older group (Age × Congruence interaction, F
Discussion
The present study aimed at comparing brain activity in young and older adults during fast processing of objects in natural scenes. Accuracy on the categorization task was equivalent between young and older participants for congruent scenes, and both age groups showed impaired performance when objects were embedded in incongruent contexts. Within-subject drop of performance due to scene incongruence (in terms of accuracy and RT) was more pronounced in older relative to young participants, in
CRediT authorship contribution statement
F. Rémy: Funding acquisition, Methodology, Conceptualization, Formal analysis, Writing - original draft, Writing - review & editing. N. Vayssière: Methodology, Data curation, Formal analysis, Writing - review & editing. L. Saint-Aubert: Methodology, Data curation, Writing - review & editing. N. Bacon-Macé: Methodology, Data curation. J. Pariente: Data curation. E. Barbeau: Funding acquisition, Writing - review & editing. M. Fabre-Thorpe: Funding acquisition, Methodology, Writing - review &
Acknowledgements
Research was supported by the French Agency for Research “Neurosciences, Neurologie et Psychiatrie” program ANR-08-MNPS-001-01. The authors are grateful to Denis Fize for help with creating stimuli, and to Laetitia Brault and Pauline Maruque for help with running MRI experiments. We thank Hélène Gros, Lucette Foltier and Jean-Pierre Désirat for help with participants’ scanning at the MRI platform of ToNIC INSERM and ‘Institut des Sciences du Cerveau, du Comportement et de la Cognition de
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