A virtual water maze revisited: Two-year changes in navigation performance and their neural correlates in healthy adults

Abstract

Age-related declines in spatial navigation are associated with deficits in procedural and episodic memory and deterioration of their neural substrates. For the lack of longitudinal evidence, the pace and magnitude of these declines and their neural mediators remain unclear. Here we examined virtual navigation in healthy adults (N=213, age 18–77 years) tested twice, two years apart, with complementary indices of navigation performance (path length and complexity) measured over six learning trials at each occasion. Slopes of skill acquisition curves and longitudinal change therein were estimated in structural equation modeling, together with change in regional brain volumes and iron content (R2* relaxometry). Although performance on the first trial did not differ between occasions separated by two years, the slope of path length improvement over trials was shallower and end-of-session performance worse at follow-up. Advanced age, higher pulse pressure, smaller cerebellar and caudate volumes, and greater caudate iron content were associated with longer search paths, i.e. poorer navigation performance. In contrast, path complexity diminished faster over trials at follow-up, albeit less so in older adults. Improvement in path complexity after two years was predicted by lower baseline hippocampal iron content and larger parahippocampal volume. Thus, navigation path length behaves as an index of perceptual-motor skill that is vulnerable to age-related decline, whereas path complexity may reflect cognitive mapping in episodic memory that improves with repeated testing, although not enough to overcome age-related deficits.

The application of a rodent-based Morris water maze (MWM) protocol to an investigation of age-related differences in human spatial learning.

“…This covariate was regarded as a direct behavioral measure of the level of visuomotor control in using the joystick to head toward a visible virtual target and was used to control for potential age group differences in joystick control. The inclusion of this covariate was also commensurate with its use as a control measure in a recent study on longitudinal change in vMWM search performance (see Daugherty & Raz, 2017). …”

Striatal iron content is linked to reduced fronto-striatal brain function under working memory load

“…Brain iron accumulation is observed continuously across the adult lifespan (Hallgren and Sourander 1958;Rodrigue et al 2011;Raz 2013, 2017). However, the majority of extant evidence for its use as a biomarker included outcomes that show meaningful agerelated decline after the fifth decade-namely, regional brain volume and cognitive deficit (e.g., Sullivan et al, 2009;Rodrigue et al, 2013;Daugherty & Raz, 2017). Nonetheless, prominent theories of brain iron accumulation as Iron and BOLD modulation 16 a harbinger of neurodegeneration, including the Free Radical Induced Energetic and Neural Decline in Senescence model (FRIENDS; Raz & Daugherty, 2018), posit functional disruption that may precede structural and cognitive decline.…”

“…Within adult lifespan samples of healthy aging, greater brain iron concentration predicts agerelated volumetric shrinkage over 2 years and up to 7 years later (Daugherty and Raz 2016). Age-related increase in iron is detrimental to regionspecific functions, including episodic memory (Rodrigue et al 2013), working memory and executive function (Pujol et al 1992;Bartzokis et al 2011;Ghadery et al 2015), spatial navigation ability (Daugherty and Raz 2017), and psychomotor speed (Sullivan et al 2009) and control (Adamo et al 2014). Further, iron accumulation over short periods predicts age-related neurodegenerative disease progression and symptom severity (Ulla et al 2013;Walsh et al 2013).…”

Spatial memory and navigation in ageing: A systematic review of MRI and fMRI studies in healthy participants

“…Wayne State University, consisting of two (Moffat, Elkins, & Resnick, 2006;Moffat, Kennedy, Rodrigue, & Raz, 2007) and three studies Daugherty, Bender, Yuan, & Raz, 2016;Daugherty & Raz, 2017) respectively. Details of the studies and the main findings are presented, separately for MRI and fMRI, in Tables 3a and 3b.…”

“…Seven studies (Antonova et al, 2009;Daugherty et al, , 2016Daugherty & Raz, 2017;Driscoll et al, 2003;Korthauer et al, 2016;Moffat et al, 2007) used virtual reality analogues, presented on computer screens and controlled by keyboard or joystick, of the Morris Water Task (vMWT), a test of spatial memory. They mainly investigated allocentric processing through randomised start points, although individual studies focused on examining different outcome measures.…”