1. Increased Hippocampal Excitability and Altered Learning Dynamics Mediate Cognitive Mapping Deficits in Human Aging
- Author
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Jose P Valdes-Herrera, Claus Tempelmann, Nadine Diersch, and Thomas Wolbers
- Subjects
Male ,Aging ,physiology [Hippocampus] ,Hippocampus ,Hippocampal formation ,Spatial memory ,physiology [Psychomotor Performance] ,memory ,methods [Brain Mapping] ,methods [Magnetic Resonance Imaging] ,0302 clinical medicine ,Cognition ,Retrosplenial cortex ,Parietal Lobe ,Function learning ,psychology [Aging] ,Aging brain ,Research Articles ,diagnostic imaging [Hippocampus] ,0303 health sciences ,Brain Mapping ,learning ,Cognitive map ,General Neuroscience ,fMRI ,physiology [Cognition] ,Virtual Reality ,Sulcus ,Middle Aged ,physiology [Aging] ,Magnetic Resonance Imaging ,diagnostic imaging [Parietal Lobe] ,medicine.anatomical_structure ,Learning dynamics ,Female ,Psychology ,Adult ,physiology [Spatial Navigation] ,Behavioral/Cognitive ,Spatial Learning ,spatial navigation ,Affect (psychology) ,03 medical and health sciences ,Young Adult ,medicine ,Humans ,ddc:610 ,030304 developmental biology ,Aged ,physiology [Spatial Learning] ,physiology [Parietal Lobe] ,aging ,Younger adults ,Neuroscience ,030217 neurology & neurosurgery ,Psychomotor Performance - Abstract
Learning the spatial layout of a novel environment is associated with dynamic activity changes in the hippocampus and in medial parietal areas. With advancing age, the ability to learn spatial environments deteriorates substantially but the underlying neural mechanisms are not well understood. Here, we report findings from a behavioral and a fMRI experiment where healthy human older and younger adults of either sex performed a spatial learning task in a photorealistic virtual environment (VE). We modeled individual learning states using a Bayesian state-space model and found that activity in retrosplenial cortex (RSC)/parieto-occipital sulcus (POS) and anterior hippocampus did not change systematically as a function learning in older compared with younger adults across repeated episodes in the environment. Moreover, effective connectivity analyses revealed that the age-related learning deficits were linked to an increase in hippocampal excitability. Together, these results provide novel insights into how human aging affects computations in the brain's navigation system, highlighting the critical role of the hippocampus.SIGNIFICANCE STATEMENTKey structures of the brain's navigation circuit are particularly vulnerable to the deleterious consequences of aging, and declines in spatial navigation are among the earliest indicators for a progression from healthy aging to neurodegenerative diseases. Our study is among the first to provide a mechanistic account about how physiological changes in the aging brain affect the formation of spatial knowledge. We show that neural activity in the aging hippocampus and medial parietal areas is decoupled from individual learning states across repeated episodes in a novel spatial environment. Importantly, we find that increased excitability of the anterior hippocampus might constitute a potential neural mechanism for cognitive mapping deficits in old age.
- Published
- 2021