Age differences in neural correlates of route encoding and route recognition
Introduction
Deficits in spatial and navigational memory are important components of aging-related changes in cognitive abilities (for review, see Kirasic, 2001). It is common that elderly individuals not only avoid unfamiliar routes and places due to self-perceived deficits in navigation (Burns, 1999), they also have measurable deficits in place and route learning as assessed in real and virtual reality environments Kirasic, 1991, Kirasic et al., 1992, Moffat and Resnick, 2002, Moffat et al., 2001, Wilkniss et al., 1997. Moreover, navigational memory deficits are an important marker of early dementia and thus relevant for early diagnosis (Morris, 1993). Thus, elderly adults encounter more difficulty in learning and remembering new routes in novel environments as compared to younger adults. However, the neural correlates of these age-related differences in route encoding and route recognition are unknown. Moreover, it is unknown whether an encoding or a retrieval deficit causes navigational deficits in old age.
In young subjects, several imaging studies have identified brain structures involved in the encoding of new and recognition of familiar environments (for review, see Burgess et al., 2002). Encoding is consistently accompanied by activation of the dorsal visual pathway reaching the parietal lobe and the ventral visual pathway extending into the medial temporal lobe (MTL). The effectiveness of navigational encoding seems to be positively correlated with inferior and medial temporal activity Aguirre and D'Esposito, 1997, Aguirre et al., 1996, Hartley et al., 2003, Iaria et al., 2003, Maguire et al., 1998a, Maguire et al., 1998b. The general relation between temporal activity and effective encoding is also well supported by studies using the subsequent memory effect, which show greater posterior fusiform/parahippocampal activity for later remembered as compared to later forgotten pictures depicting large-scale spatial layouts Brewer et al., 1998, Kirchhoff et al., 2000, Weis et al., 2004.
There is considerable overlap in brain activation observed during encoding and retrieval of navigational information. Nevertheless, recognition of learned spatial environments in a route recognition task is often accompanied by more prefrontal activations compared to encoding, including activations of the anterior cingulate cortex as well as the pre- and supplementary motor cortices (Burgess et al., 2002).
Although no functional neuroimaging study has yet investigated the neural correlates of age-related deficits in navigational memory, there are several studies that tackle age-related declarative memory deficits in general. The most consistent findings reported in these studies include a reduced encoding-related inferior and medial temporal activity in older as compared to younger subjects (e.g., Daselaar et al., 2003, Grady et al., 1995, Morcom et al., 2003, Schiavetto et al., 2002). In addition, older subjects appear to recruit additionally other brain regions, predominately in the prefrontal cortex. The recruitment of frontal regions together with the relatively diminished responses observed in the temporal lobe and other posterior regions, including the parietal cortex, is sometimes called the posterior–anterior shift (Grady et al., 2003). It has been suggested that with increasing age additional cognitive resources involving executive and organizational functions are utilized instead or in complement to the perceptually based processes engaged by younger subjects. The prefrontal activations in older subjects are often less asymmetric than in young subjects, leading Cabeza (2002) to formulate the so-called HAROLD model (Hemispheric Asymmetry Reduction in Older adults). Such reductions in asymmetry have most consistently been found in high performing older adults (Cabeza et al., 2002). Therefore, the recruitment of the homologue prefrontal region in the contralateral hemisphere has been regarded as a mechanism for compensating age-related deficits in other brain regions including the temporal lobe Cabeza et al., 2002, Daselaar et al., 2003, Dolcos et al., 2002, Grady and Craik, 2000, Logan et al., 2002. In contrast, in some circumstances, under-recruitment of frontal regions has also been observed in elderly, perhaps indicating that elderly might be less likely to self-initiate the most effective strategy for solving a given task Cabeza et al., 1997, Grady et al., 1995, Logan et al., 2002.
Summing up the current status, older adults often show a navigational memory deficit, the neural correlates of route encoding and recognition are well studied in young subjects, and studies comparing brain activity related to mnemonic operations between younger and older adults have found consistent differences. However, the neural correlates of age-related deficits in navigational memory are, to our knowledge, yet unstudied. To tackle this issue, we investigated 20 elderly and 20 young healthy subjects by fMRI while they performed a virtual reality spatial memory task including route encoding and route recognition conditions.
Section snippets
Participants
Forty healthy volunteers participated in the study (20 young subjects, 10 female; mean age = 23 years, SD = 2.8, range 18–29; 20 old subjects, 10 female; mean age = 63 years, SD = 7.2, range 53–78). All but two young and two old subjects were right-handed as indexed by an Edinburgh handedness index of ≥90 (Oldfield, 1971). The mean number of years of formal education was 16 (SD = 2.0) for old and 16 (SD = 0.4) for young subjects. Dutch was the first language in all subjects. All subjects were
Behavioral results
The subject performance during route recognition was well above chance level (50%) in both groups (young: mean correct = 79.5%, SD = 12.0, t19 = 11.0, P < 0.0001; old: mean correct = 73.3%, SD = 16.8, t19 = 6.2, P < 0.0001). Young subjects performed slightly but significantly better than old subjects (t38 = 1.3, P < 0.05).
Route encoding vs. visuomotor control condition
In young and old subjects, learning routes through unfamiliar virtual environments significantly activated relative to the visuomotor control condition distributed regions in
Discussion
The behavioral results indicate that both groups of subjects were able to learn and effectively solve the recognition task. However, there was a small but significant difference in performance between groups. It is likely that this difference is attributable to subtle spatial memory deficits in our sample of older subjects, consistent with previous findings (Kirasic, 1991, Kirasic et al., 1992, Moffat and Resnick, 2002, Moffat et al., 2001, Wilkniss et al., 1997; for review, see Kirasic, 2001).
Acknowledgements
We thank Paul Gaalman for professional technical assistance in data acquisition.
References (63)
- et al.
Hippocampal formation
- et al.
The human hippocampus and spatial and episodic memory
Neuron
(2002) - et al.
Aging gracefully: compensatory brain activity in high-performing older adults
NeuroImage
(2002) - et al.
Mediators of age-related differences in recollective experience in recognition memory
Acta Psychol.
(2002) - et al.
Hemispheric asymmetry and aging: right hemisphere decline or asymmetry reduction
Neurosci. Biobehav. Rev.
(2002) - et al.
Thresholding of statistical maps in functional neuroimaging using the false discovery rate
NeuroImage
(2002) - et al.
Coexistence of attention-based facilitation and inhibition in the human cortex
NeuroImage
(1998) - et al.
The irrelevant speech effect: a pet study
Neuropsychologia
(2003) - et al.
Changes in memory processing with age
Curr. Opin. Neurobiol.
(2000) - et al.
Activation of the human hippocampal formation during auditory-verbal long-term memory function
Neurosci. Lett.
(1993)
The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans
Neuron
Under-recruitment and nonselective recruitment: dissociable neural mechanisms associated with aging
Neuron
Object vision and spatial vision: two cortical pathways
Trends Neurosci.
Age differences in spatial memory in a virtual environment navigation task
Neurobiol. Aging
The assessment and analysis of handedness: the Edinburgh inventory
Neuropsychologia
Effective auditory-verbal encoding activates the left prefrontal and medial temporal lobes: a generalization to illiterate subjects
NeuroImage
Dynamic changes in the functional anatomy of the human brain during recall of abstract designs related to practice
Neuropsychologia
Neural correlates of memory for object identity and object location: effects of aging
Neuropsychologia
‘What’ and ‘where’ in the human brain
Curr. Opin. Neurobiol.
Analysis of fMRI time-series revisited-again
NeuroImage
The Geometry of Random Fields
Environmental knowledge is subserved by separable dorsal/ventral neural areas
J. Neurosci.
The parahippocampus subserves topographical learning in man
Cereb. Cortex
Making memories: brain activity that predicts how well visual experience will be remembered
Science
Recognition memory: what are the roles of the perirhinal cortex and hippocampus?
Nat. Rev., Neurosci.
Navigation and the mobility of older drivers
J. Gerontol., B Psychol. Sci. Soc. Sci.
Hemispheric asymmetry reduction in older adults: the HAROLD model
Psychol. Aging
Age-related differences in effective neural connectivity during encoding and recall
NeuroReport
Neural systems for visual orienting and their relationships to spatial working memory
J. Cogn. Neurosci.
Neuroanatomical correlates of episodic encoding and retrieval in young and elderly subjects
Brain
Neuropsychological correlates of recollection and familiarity in normal aging
Cogn. Affect. Behav. Neurosci.
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