No other memory measure revealed significant associations with HC-maturity scores Table S1.
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Both mnemonic similarity judgments and the rejection of foils in a recognition memory task involving highly similar items crucially depend on the orthogonalization of overlapping feature sets in representational space. Therefore, our results suggest that the multidimensional maturity of structures in the HC is specifically related to processes that enable the construction of unique mnemonic representations of highly overlapping feature sets during memory encoding. Conversely, the present results also suggest that age-associated differences in item memory, source memory, and associative memory performance Fig.
S1 depend less on HC maturity than the age-associated changes in the disambiguation of highly similar events. Clearly, performance on item memory, source memory, and associative memory relates to hippocampal functioning However, the demand characteristics of these tasks, under most conditions at least, presumably depend less on pattern separation than the demand characteristics of making mnemonic similarity judgments and rejecting highly similar foils.
This enhanced prefrontal dependence may inject additional age-related variance into task performance, which may weaken or mask potential associations with HC maturity.
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S2 for methods. A Six frontal ROIs defined by the lpba40 atlas B Latent variable weights brain saliences for each ROI used to transform individual GM volumetric estimates, extracted using VBM, into one latent variable expressing the largest amount of information common to the multivariate pattern of GM and age.
Z score-like values of stability suggest a negative relationship between all ROIs and age. C The resulting latent variable, termed frontal maturity score, plotted against age. Increasing frontal maturity related to an increase in source memory accuracy D and increase in correct item recognition E. C — E Dashed lines represent least-square lines. Related to Fig. Scatterplots showing performance in percent on memory scores derived from the two behavioral tasks Fig. Red lines represent linear regression models fit on the relationship of performance with age.
Two separate images [field of view FOV : mm; repetition time TR : 6, ms; echo time TE : 16 ms; number of slices: 30; voxel size: 0. Subfields were traced on all volumes by both tracers A.
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First, one tracer traced half of the slices for a given volume, and then the other tracer traced the remaining slices. Raters were blind to participant age. In demarcation of the ROIs, we followed suggestions by refs. Specifically, in comparison with Shing et al. We defined ranges for the body similarly to Lee et al. Bilateral ROIs were collapsed across hemisphere for all following analyses. To account for differences in ROI volumes because of differences in head size, we used the analysis of covariance approach 59 , 60 with a slight modification to avoid negating age effects on ROIs.
We adjusted all ROI volumes in two steps. The adjusted volumetric data are used for all ROIs throughout the present report. In the mnemonic similarity task Fig.
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They saw pictures, each for 2, ms with an intertrial interval jittered with a left-skewed distribution between 1, and 2, ms , with objects shown only once, 72 objects repeated once with exactly the same picture, and 72 objects repeated with a slightly different picture. Repetition lags for repeated objects were 15, 20, 25, and 30 trials.
The encoding phase was organized in six blocks with two contexts alternating for a later source memory task. Contexts were presented by a short video before each block.
Again, they saw a series of pictures depicting objects, targets i. Each trial was shown for 1, ms, with an ITI of 2, ms for young adults, and 5, ms for children, with a total response window of 3, ms and 6, ms, respectively. Assignment of pictures to conditions and blocks to contexts, and order of presentation, was pseudorandomized for each participant with the above constraints.
A bias score closer to zero would suggest a bias toward pattern completion, whereas a score closer to one would suggest a bias toward separation. A given score does not allow for inferring whether a given value means more pattern separation than completion; however, the difference in two scores suggests differential biases between separation and completion. Trials that were responded either similar or old were followed by a source memory decision trial, where participants had to choose the source of the item during encoding from two response options source 1 vs.
Here, all target and lure items were pooled together to provide an overall accuracy score that served as our source memory measure. In the faces and names task Fig. During encoding 36 trials, 3, ms each, with a ms ITI participants saw 18 male and 18 female faces, presented with corresponding high-frequency names. They were instructed to report their subjective decision on whether the name did or did not fit the face. After a 1-min delay, participants performed a surprise recognition test that consisted of three phases, presented in a random order: an item test for faces, an item test for names, and an associative test for face-name pairs.
Sets were then randomly assigned to test phases.
In each test phase, 12 targets from the assigned set and 12 novel foils were presented, each for 4, ms. This design ensured that no item appeared more than once during the test, and also that no item appeared again in a test phase if its paired associate had been presented in another test phase. The associative test included only faces and names presented during encoding that were either paired as during encoding or rearranged. For the item tests, participants were instructed to indicate whether an item was old or new.
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For the associative test, they were instructed to respond old to nonrearranged pairs, and new to rearranged pairs. Results for two item test phases faces and names were pooled together for the analyses. Except for pattern separation, there is also existing data suggesting that these processes undergo some form of development Using multivariate correlational techniques on high-resolution structural MRI data of the MTL in a sample of 6- to y-old individuals, we identified a multivariate profile of developmental differences in HC substructures that expresses the structural maturity of the HC.
We then showed that HC maturity is specifically related to the development of memory processes promoting the unique encoding of overlapping memory representations. Our results suggest that key contributors of this specific connection between HC maturity and memory are age-associated changes in the DG-CA3 and the EC. HC maturity scores did not reveal a robust association with any of the other memory measures, although these measures also showed age-associated improvements Fig.
Pedro M. Paz-Alonso, Silvia A. Bunge, and Simona Ghetti
The mnemonic similarity task has been specifically designed to assess this bias on a continuous scale between separation and completion 37 , whereas performance on the other memory measures may more heavily depend on extrahippocampal areas not incorporated in our HC-maturity score 23 , 25 , Our observation that the association between HC maturity and memory is restricted to age-related increases in specificity may reflect one or both of the following underlying processes.
First, the development of memory processes that require less specificity with regard to unique feature combinations may depend more strongly on age-related changes in extrahippocampal areas. As discussed above, maturation of prefrontal cortex can, in part, drive improvements in both associative recognition memory and source memory 23 , 25 , 26 , possibly moderated by increases in demands on strategic processes rather than associative memory operations However, we should note that, based on standard-resolution MRI, some studies have found age differences in the functional division along the longitudinal axis of the HC 27 , 28 that may also contribute to age differences in source memory ability Second, pattern completion may be relatively mature by middle childhood despite ongoing structural changes in HC, whereas computations underlying specificity are still developing, thus promoting the observed age-graded shift in bias from pattern completion to pattern separation.
Our results complement earlier findings 14 demonstrating age-associated differences in HC subfields in middle childhood and extend those observations to a large sample of children aged 6 to 14 y. In addition, we provide an initial picture of HC subfield development in middle childhood. This picture highlights the presence of subfield-specific, heterogeneous maturational tracks. By demonstrating that estimates of whole HC volumes failed to detect HC-age associations in our sample, the results of the present study also help to resolve conflicting observations, with some studies suggesting that HC maturation levels off early in middle childhood 8 , 13 , 31 , 34 and others suggesting that HC maturation extends well into, and possibly beyond, this period 7.
Previously available standard resolution MRI techniques may not be sensitive enough to reveal extended HC maturation. Our study revealed effects that complement earlier studies linking the DG and CA3 to pattern separation 6 , 10 , Beyond the crucial role of the DG-CA3 region for providing separable inputs to downstream HC subfields, the development of memory specificity appears associated with a common maturational process that potentially affects all HC subfields to varying degrees.
Our finding that EC development is a key component of HC maturity associated to pattern separation fits nicely with observations in animals that layer 2 and 5 of the lateral EC follows DG development 20 , and with human data suggesting that lateral EC may perform pattern separation on overlapping object representations before passing its input onto the DG It is worth noting that EC by itself did not show significant age-related differences in the present sample.
The contribution of EC to HC maturity was revealed only when applying a multivariate approach that expresses the common variance between individual differences in HC subfield volumes and age. Methodologically, our approach follows the longstanding claim to conceptualize and analyze developmental change from a multivariate perspective Earlier work has shown that multivariate composites of individual differences in brain anatomy can serve as a summary description of biological maturity The dimensionality reduction associated with these methods helps to test and refine theories of age-graded changes in brain—behavior relations.
The present study has several limitations, which can guide future research in the field. Given that development is a process unfolding in ontogenetic time, repeated within-subjects assessments are needed to directly capture longitudinal relationships between neural and behavioral variables of interest For this reason, we refrained from using hierarchical linear regression models with age as independent variable, memory processes as dependent variables, and HC subfields as mediator variables.
It has been shown analytically that these methods may fail to detect longitudinal mediation when it is present false negatives and detect mediation when it is absent false positives 47 ; see also ref. A second limitation is related to the bias score used in this study, which pits pattern separation against pattern completion. Future studies need to obtain measures that separately index age differences in the efficiency of pattern separation and pattern completion mechanisms.
The restriction of our analyses to HC body is a third limitation. Previous studies found both structural and functional age-related differences in source memory contributions of the HC head and tail, but not the body 27 , Investigating subfield contributions along the full anatomical extent of HC could therefore refine our understanding of how HC subfield and memory development are related see ref.
Fourth, recent fMRI findings suggest that pattern separation may not be restricted to the HC 50 , In the present study, we selected a task that aims at studying age differences in pattern separation performed by the HC, but one that is not well-suited for examining pattern separation, and age differences therein, in other brain areas, such as visual cortex.
Future studies need to address the maturational course of pattern separation in other brain areas and their contributions to behavioral development. Last, we devised this study to test the suggestion that HC and related mnemonic functions may develop beyond the onset of middle childhood, but had no a priori reason to postulate that this development may continue beyond middle childhood. Therefore, we did not include individuals aged 15—18 y in the present sample.
Also, we did not include children below 6 y of age, reflecting practical limitations when conducting MRI studies with young children. Our results should encourage future research to explore HC subfields and related mnemonic development in a more extended age range. We found that age-related shifts from pattern completion toward pattern separation are associated with maturational changes in HC subfields. If corroborated by longitudinal evidence from tasks directly measuring some form of knowledge extraction from invariances i.
Participants provided written informed consent, also signed by the primary caregiver for all children. Participants were right-handed and had no history of neurological or psychiatric disorders. Behavioral data were not available for one child and one young adult because of technical issues. Four ROIs were manually demarcated bilaterally Fig. First, deciphering the role of various subregions in memory has proven difficult because the HC forms a hard-wired interconnected processing circuit of interdependent nodes. By extracting a latent HC subfield profile that maximally shares common variance with age, we aimed at increasing precision for sampling from a latent maturational process.
Third, while univariate analyses can capture age-related differences in subregions separately, they ignore intercorrelated patterns of developmental processes affecting the different subparts in a concerted fashion. Significance of the detected association was assessed by using 5, permutation tests of the singular value corresponding to the LV.
A subsequent bootstrapping procedure revealed the robustness of within-LV ROI weights across 5, bootstrapped resamples of the data. Results of this analysis are presented in Fig. We used the standard preprocessing pipeline of the CAT12 toolbox dbm. Regardless of the perspective adopted there are hundreds of specialties that psychologists practice. These specialties can usually be grouped into general fields. The first use of the term "psychology" is often attributed to the German scholastic philosopher Rudolf Goeckel Latinized Rudolph Goclenius , published in The term did not fall into popular usage until the German idealist philosopher, Christian Wolff used it in his Psychologia empirica and Psychologia rationalis This distinction between empirical and rational psychology was picked up in Diderot's Encyclopedie and was popularized in France by Maine de Biran.