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The Journal of Neuroscience, September 8, 2004, 24(36):7939-7944; doi:10.1523/JNEUROSCI.0703-04.2004

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Behavioral/Systems/Cognitive
Age-Related Functional Changes of Prefrontal Cortex in Long-Term Memory: A Repetitive Transcranial Magnetic Stimulation Study

Simone Rossi,^1,2 Carlo Miniussi,² Patrizio Pasqualetti,³ Claudio Babiloni,^2,4 Paolo M. Rossini,^3,5 and Stefano F. Cappa⁶

¹Dipartimento di Neuroscienze, Sezione Neurologia, Università di Siena, I-53100 Siena, Italy, ²Istituto di Ricovero e Cura a Carattere Scientifico S. Giovanni di Dio Fatebenefratelli, I-25125 Brescia, Italy, ³Associazione Fatebenefratelli per la Ricerca-Dipartimento di Neuroscienze, S. Giovanni Calibita, Fatebenefratelli Isola Tiberina, I-00186 Roma, Italy, ⁴Dipartimento di Fisiologia Umana e Farmacologia, Università La Sapienza, I-00185 Roma, Italy, ⁵Clinica Neurologia, Università Campus Biomedico, I-00185 Roma, Italy, and ⁶Centro di Neuroscienze Cognitive, Università Salute-Vita S. Raffaele, I-20132 Milano, Italy

Neuroimaging findings suggest that the lateralization of prefrontal cortex activation associated with episodic memory performance is reduced by aging. It is still a matter of debate whether this loss of asymmetry during encoding and retrieval reflects compensatory mechanisms or de-differentiation processes. We addressed this issue by the transient interference produced by repetitive transcranial magnetic stimulation (rTMS), which directly assesses causal relationships between performance and stimulated regions. We compared the effects of rTMS (a rapid-rate train occurring simultaneously to the presentation of memoranda) applied to the left or right dorsolateral prefrontal cortex (DLPFC) on visuospatial recognition memory in 66 healthy subjects divided in two classes of age (<45 and >50 years).

In young subjects, rTMS of the right DLPFC interfered with retrieval more than left DLPFC stimulation. The asymmetry of the effect progressively vanished with aging, as indicated by bilateral interference effects on recognition performance. Conversely, the predominance of left DLPFC effect during encoding was not abolished in elders, thus probing its causal role for encoding along the life span. Findings confirm that the neural correlates of retrieval modify along aging, suggesting that the bilateral engagement of the DLPFC has a compensatory role on the elders' episodic memory performance.

Key words: long-term memory; neuroimaging; transcranial magnetic stimulation; rTMS; prefrontal cortex; hippocampal formation; aging

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Received Feb 27, 2004; revised July 17, 2004; accepted July 19, 2004.

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