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Reassessing the HAROLD model: Is the hemispheric asymmetry reduction in older adults a special case of compensatory-related utilisation of neural circuits?

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Abstract

The HAROLD (hemispheric asymmetry reduction in older adults) model, proposed by Cabeza in 2002, suggests that age-related neurofunctional changes are characterised by a significant reduction in the functional hemispheric lateralisation in the prefrontal cortex (PFC). The supporting evidence, however, has been derived from qualitative explorations of the data rather than from explicit statistical assessments of functional lateralisation. In contrast, the CRUNCH (compensation-related utilisation of neural circuits hypothesis) model posits that elderly subjects recruit additional brain regions that do not necessarily belong to the contralateral hemisphere as much as they rely on additional strategies to solve cognitive problems. To better assess the validity and generalisability of the HAROLD model, we analysed the fMRI patterns of twenty-four young subjects (age range: 18–30 years) and twenty-four healthy elderly subjects (age range: 50–80 years) collected during the performance of two linguistic/semantic tasks (a picture-naming task and a sentence judgment task) and two episodic long-term memory (eLTM) recognition tasks for the same materials. The functional hemispheric lateralisation in each group and the ensuing between-group differences were quantitatively assessed using statistical lateralisation maps (SLMs). The number of clusters showing a genuine HAROLD effect was proportional to the level of task demand. In addition, when quantitatively significant, these effects were not restricted to the PFC. We conclude that, in its original version, the HAROLD model captures only some of the age-related brain patterns observed in graceful ageing. The results observed in our study are compatible with the more general CRUNCH model, suggesting that the former patterns can be considered a special manifestation of age-related compensatory processes.

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Notes

  1. This acronym stands for hemispheric asymmetry reduction in older adults. The papers in which the model has been proposed have been cited approximately 1,500 times in a decade.

  2. In the literature on ageing, the term “compensation” refers to the overactivation of new (when compared to juvenile patterns) brain regions (e.g. prefrontal cortex and posterior parietal cortex) in association with the maintenance of a good level of performance (Grady 2008), while with the term “dedifferentiation” the authors refer to the less efficient neuromodulation of brain networks, which would cause less distinctive neuronal representations (Li and Sikstrom 2002).

  3. In Cabeza et al. (2002) the HAROLD effect was demonstrated during the recall phase of two episodic memory tasks in high-performing elderly subjects.

  4. The brain regions showing an asymptotic response in the elderly were the occipital cortex, the PFC and the dorso-lateral parietal cortex (Schneider-Garces et al. 2010).

  5. The template used during the normalisation phase was a custom-made symmetrical template derived from the data of 40 normal healthy subjects aged between 18 and 40 years. The symmetrical template was obtained by averaging the right-is-right and left-is-right mean stereotactically normalised images obtained from the 40 subjects after their normalisation to the EPI template distributed with SPM2.

  6. It is important to note that we adopted block design analyses, that is, we compared the neural activations triggered by the experimental stimuli with those elicited by the baseline stimuli, and we did not isolate the events related to target detection from the time series. Accordingly, the activation patterns reflect the general cognitive process elicited by each task of interest.

  7. The statistical threshold was set at p < 0.001 to emulate the analysis of the first neurofunctional study designed to explore the HAROLD model (Cabeza et al. 2002).

  8. Cabeza (2002) acknowledges that there would be situations in which a HAROLD pattern would be missed unless a formal voxel-wise assessment was performed. For example, if “the PFC activity is below threshold in both groups … an age-related asymmetry reduction is likely to be missed unless specifically tested”.

  9. Patterns that seemed to be age specific were described on the basis of the mere observation of the topography of simple (in statistical terms) effects of brain activations rather than the proper age-by-hemisphere interaction effects.

  10. In the discussion, we sometimes refer to HAROLD rather than to the HAROLD model with much the same attitude, whereby one looks for acronyms that can be easily memorised, such as those that result in a proper name, like HAROLD does.

Abbreviations

CRUNCH:

Compensation-related utilisation of neural circuits hypothesis

eLTM:

Episodic long-term memory

fMRI:

Functional magnetic resonance imaging

HAROLD:

Hemispheric asymmetry reduction in older adults

HERA:

Hemispheric encoding/retrieval asymmetry

LI:

Laterality index

PFC:

Prefrontal cortex

PNT:

Picture-naming task

PRT:

Picture recognition task

ROI:

Region of interest

SJT:

Sentence judgment task

SLM:

Statistical lateralisation map

SRT:

Sentence recognition task

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Acknowledgments

This work was presented at the 28th European Workshop on Cognitive Neuropsychology (Bressanone, Italy, January 2010). Part of this work was included in the PhD thesis defended by MB in January 2010. The statistical analyses were run and the paper was written, in part, while the first author (MB) was funded by the University of Milano-Bicocca and “Dote Ricercatori”: FSE, Regione Lombardia, Italy.

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Correspondence to Manuela Berlingeri.

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Berlingeri, M., Danelli, L., Bottini, G. et al. Reassessing the HAROLD model: Is the hemispheric asymmetry reduction in older adults a special case of compensatory-related utilisation of neural circuits?. Exp Brain Res 224, 393–410 (2013). https://doi.org/10.1007/s00221-012-3319-x

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