The distinctiveness of neural information representation is crucial for successful memory performance but declines with advancing age. Computational models implicate age-related neural dedifferentiation on the level of item representations, but previous studies mostly focused on age differences of categorical information representation in higher-order visual regions. In an age-comparative fMRI study, we combined univariate analyses and whole-brain searchlight pattern similarity analyses to elucidate age differences in neural distinctiveness at both category and item levels and their relation to memory. Age-related neural dedifferentiation was shown as reduced category-selective processing in ventral visual cortex and impoverished item specificity in occipital regions. Importantly, successful subsequent memory performance built upon high item stability which was greater in younger than older adults. Finally, we identified a multivariate profile of neural distinctiveness across representational levels that captured both age group and recognition performance differences, emphasizing that neural dedifferentiation is a generalized phenomenon in the aging brain.

Age-related memory decline is associated with changes in neural functioning, but little is known about how aging affects the quality of information representation in the brain. Whereas a long-standing hypothesis of the aging literature links cognitive impairments to less distinct neural representations in old age ("neural dedifferentiation"), memory studies have shown that overlapping neural representations of different studied items are beneficial for memory performance. In an electroencephalography (EEG) study, we addressed the question whether distinctiveness or similarity between patterns of neural activity supports memory differentially in younger and older adults. We analyzed between-item neural pattern similarity in 50 younger (19-27 years old) and 63 older (63-75 years old) male and female human adults who repeatedly studied and recalled scene-word associations using a mnemonic imagery strategy. We compared the similarity of spatiotemporal EEG frequency patterns during initial encoding in relation to subsequent recall performance. The within-person association between memory success and pattern similarity differed between age groups: For older adults, better memory performance was linked to higher similarity early in the encoding trials, whereas young adults benefited from lower similarity between earlier and later periods during encoding, which might reflect their better success in forming unique memorable mental images of the joint picture-word pairs. Our results advance the understanding of the representational properties that give rise to subsequent memory, as well as how these properties may change in the course of aging.

SummaryThe distinctiveness of neural information representation is crucial for successful memory performance but declines with advancing age. Computational models implicate age-related neural dedifferentiation on the level of item representations, but previous studies mostly focused on age differences of categorical information representation in higher-order visual regions. In an age-comparative fMRI study, we combined univariate analyses and whole-brain searchlight pattern similarity analyses to elucidate age differences in neural distinctiveness at both category and item levels and their relation to memory. Age-related neural dedifferentiation was shown as reduced category-selective processing in ventral visual cortex and impoverished item specificity in occipital regions. Importantly, successful subsequent memory performance built upon high item stability which was greater in younger than older adults. Finally, we identified a multivariate profile of neural distinctiveness across representational levels that captured both age group and recognition performance differences, emphasizing that neural dedifferentiation is a generalized phenomenon in the aging brain.

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Perceiving the geometry of surrounding space is a multisensory process, crucial to contextualizing object perception and guiding navigation behavior. Humans can make judgments about surrounding spaces from reverberation cues, caused by sounds reflecting off multiple interior surfaces. However, it remains unclear how the brain represents reverberant spaces separately from sound sources. Here, we report separable neural signatures of auditory space and source perception during magnetoencephalography (MEG) recording as subjects listened to brief sounds convolved with monaural room impulse responses (RIRs). The decoding signature of sound sources began at 57 ms after stimulus onset and peaked at 130 ms, while space decoding started at 138 ms and peaked at 386 ms. Importantly, these neuromagnetic responses were readily dissociable in form and time: while sound source decoding exhibited an early and transient response, the neural signature of space was sustained and independent of the original source that produced it. The reverberant space response was robust to variations in sound source, and vice versa, indicating a generalized response not tied to specific source-space combinations. These results provide the first neuromagnetic evidence for robust, dissociable auditory source and reverberant space representations in the human brain and reveal the temporal dynamics of how auditory scene analysis extracts percepts from complex naturalistic auditory signals.