Edited by: Hari S. Sharma, Uppsala University, Sweden
Reviewed by: John F. Disterhoft, Northwestern University Medical School, USA; Ashok K. Shetty, Duke University Medical Center, USA
*Correspondence: Maria Cotelli, Istituto Di Ricovero e Cura a Carattere Scientifico, Centro San Giovanni di Dio Fatebenefratelli, Via Piastroni, 4 25125 Brescia, Italy. e-mail:
This is an open-access article subject to an exclusive license agreement between the authors and the Frontiers Research Foundation, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.
Word-retrieval difficulties commonly occur in healthy aging. Recent studies report an improved ability to name pictures after the administration of high-frequency repetitive transcranial magnetic stimulation (rTMS) in healthy younger adults and in patients with neurological disease. The aim of this study was to assess the effect of high-frequency rTMS applied to the dorsolateral prefrontal cortex (DLPFC) on picture naming in healthy older adults. High-frequency rTMS was applied to the left and right DLPFC during object and action naming in 13 healthy older adults. The naming latency for actions was shortened after stimulation of the left and right DLPFC compared to application of the sham stimulation. Stimulation was not observed to have any effect on correctness of naming. Our data demonstrate the involvement of the left and right DLPFC in a sample of healthy aging subjects during an action-naming task. The bilateral involvement of the DLPFC in these participants is discussed together with data on younger adults and on Alzheimer's patients.
Several studies have investigated cognitive changes linked to healthy aging and have documented an age-related decline in naming (Goodglass,
Naming difficulty is commonly present in aphasic and demented patients (Robinson et al.,
Repetitive transcranial magnetic stimulation (rTMS) can induce a brief change in a subject's behavioral performance only if it is applied over an area that is causally engaged in that task being executed. Recent studies reported an improved ability to name pictures after the administration of rTMS over the prefrontal cortex in healthy younger adults and in patients with several types of neurological diseases (Topper et al.,
The purpose of this study was to explore the effects of rTMS applied to the DLPFC on an action and object picture-naming task in older adults. We hypothesized that stimulation of the left DLPFC can generate a facilitatory effect, namely a decrease in the verbal reaction time in action picture naming, as previously found in younger adults. Furthermore, if physiological aging implies hemispheric asymmetry reduction, as previously suggested, we would expect to find facilitation after stimulation of either the left or right DLPFC, as found in previous studies with AD patients (Cotelli et al.,
The aim of Experiment 1 was to select from a larger set of pictures a congruent subset of stimuli balanced for all variables and verbal reaction time (vRT).
Prior to being enrolled in the experiment, participants were administered a standard health history questionnaire and completed a Mini Mental State Examination (MMSE) (Folstein et al.,
The stimuli used in the action and object picture-naming tasks were taken from the Center for Research in Language-International Picture-Naming Project corpus CRL-IPNP (Bates et al.,
In Experiment 1, we used 54 objects and 54 actions taken from the CRL-IPNP database. None of the action stimuli included in the task were associated with the selected objects. The nouns and verbs corresponding to the set of objects and actions used were matched for target word frequency and length. The frequency, length of the target word, visual complexity and imageability of the pictures were matched and counterbalanced between the experimental blocks. Ten additional objects and actions were used for a practice block (5 actions and 5 objects).
Subjects sat in front of a 17-inch monitor controlled by a personal computer running Presentation software
The 54 actions were, on average, named after 1132 ms (±280), whereas the 54 objects required 823 ms (±154) to be correctly named. The mean accuracy was 90% (±14) for actions and 97% (±4) for objects.
Based on these results, we decided to exclude the actions that required a vRT higher than 1692 ms (i.e., mean vRT plus 2 standard deviations) or with a mean accuracy lower than 85%. We excluded objects with vRTs higher than 1131 (i.e., mean vRT plus 2 standard deviations) or with a mean accuracy lower than 90%.
The obtained subset of stimuli comprised 42 actions and 42 objects. Within this final set, actions were named after 1070 ms (±252), whereas objects required 777 ms (±108) to be correctly named. The mean accuracy was 95% (±5) for actions and 99% (±2) for objects. The new sets of stimuli were still matched for frequency and length.
All the exclusion criteria used in Experiment 1 were also used in Experiment 2. In addition, a neuropsychological battery was applied, and a pathological score in at least one of the tests was a further exclusion criterion. Thirteen (4 male, 9 female) healthy older adults (age 65–78 years, mean 70.2 years, education mean = 13.8 years) participated in the rTMS experiment. All participants were native Italian speakers and had normal or corrected-to-normal vision. All participants were right-handed (Oldfield,
The neuropsychological test battery included measures to assess non-verbal reasoning (Raven-Colored Progressive Matrices), language comprehension (Token Test), verbal fluency (phonemic and semantic), memory (Story Recall, Rey–Osterrieth Complex Figure Recall, Digit Span, Spatial Span), visuo-spatial abilities (Rey–Osterrieth Complex Figure, Copy), attention and executive functions (Trail-Making Test A and B). All the tests were administered and scored according to standard procedures (Lezak et al.,
Raw scores | Cut-off | |
---|---|---|
MMSE | 29.5/30 | 24 |
Raven-colored progressive matrices | 30.9/36 | 17.5 |
Story recall | 15.2/28 | 7.5 |
Rey–Osterrieth complex figure, recall | 14.6/36 | 9.46 |
Digit span | 5.7 | 3.75 |
Spatial span | 4.9 | 3.55 |
Rey–Osterrieth complex figure, copy | 33.1/36 | 28.87 |
Trail-making test A (s) | 40.2 | 93 |
Trail-making test B (s) | 117.1 | 282 |
Token test | 33.6/36 | 26.5 |
Fluency, phonemic | 39.6 | 16 |
Fluency, semantic | 45.3 | 24 |
Oral object comprehension (BADA) | 39.9/40 | |
Oral action comprehension (BADA) | 19.9/20 | |
Written object comprehension (BADA) | 39.9/40 | |
Written action comprehension (BADA) | 19.9/20 | |
Oral object naming (BADA) | 29.2/30 | |
Oral action naming (BADA) | 27.0/28 |
Experiment 2 used the 84 items (42 actions and 42 objects) selected from the previous experiment. None of the action stimuli included in this task were associated with the selected objects. The nouns and verbs corresponding to the set of objects and actions were matched for target word frequency and length.
The items were divided into three blocks designed for the three stimulation conditions (left DLPFC, right DLPFC, and sham stimulation). The frequencies and lengths of the target words were counterbalanced in the experimental blocks. The visual complexity and imageability of the pictures were also matched between blocks. Ten additional objects and actions were used for a practice block (5 actions and 5 objects).
The procedures of the behavioral task were exactly the same as those used in Experiment 1 (see Figure
We separately analyzed both vRTs and accuracy using a repeated-measures ANOVA with stimulus category (action and object) and site (sham, left and right) as factors. With respect to accuracy, this analysis only showed a significant effect of stimulus category [
The primary finding of this study is that rTMS applied to the DLPFC improves action-naming performance in older adults. This finding provides further direct evidence for a causal role of DLPFC in naming, consistent with the results of previous studies on younger adults (Cappa et al.,
In the case of language, the right hemisphere has traditionally been assigned a crucial role in supporting performance after left hemispheric damage (Vandenbulcke et al.,
The use of rTMS involves the discharge of a transient electromagnetic field through the skull. Rapidly changing magnetic fields induce electric currents in the brain, which in turn produce transynaptic depolarization of groups of neurons located in the superficial cortical layers (Heller and van Hulsteyn,
The present results showed a reduction in vRTs in action-naming performance in older adults. The reduction in vRTs suggests that this effect is related to a facilitation of the task that involves recalling the semantic representation of the action and that this facilitation speeds up task execution. Several studies have demonstrated that the reduction in naming efficacy that occurs in older adults reflects inefficient access to semantic knowledge rather than a true loss of semantic representations (Barresi et al.,
In conclusion, the present study confirms that rTMS is a useful tool that can complement traditional neuroimaging approaches in the investigation of age-dependent modifications of the causal engagement of cortical brain regions. Moreover, age-related decline in performance on an action-naming task seems to be the consequence of a slowing down of lexical access. Finally, our findings further support the HAROLD model, which posits a bilateral involvement of DLPFC in older adults compared with a left-sided involvement of this area in younger adults.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
We wish to thank the participants in the study for their patience. This research was supported by a project grant from the “Fondazione della Comunità Bresciana-onlus”.
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