This study was carried out to investigate whether anodal tDCS applied over the ATLs is effective in increasing the likelihood of the recall of proper names of famous people and places in healthy older adults. In our prior study (Ross et al., 2010
), we demonstrated that anodal tDCS can enhance the recall of proper names of famous individuals when applied over the right ATL. This effect was observed only in cases in which the names were not immediately available. This temporally selective effect on name recall is intuitive because tDCS is most likely to exhibit a modulatory effect when name retrieval is difficult. These stimulation effects are not likely due to a general arousal effect since we demonstrated selectivity across stimulation site and stimulus category.
We hypothesized that we would find an even larger effect of tDCS in this task in older subjects because of the known decline of proper name recall in normal aging (James, 2004
; James et al., 2008
). According to the transmission deficit hypothesis, normal aging is associated with a weakening of neural connections resulting in the impaired access to information with sparse connectivity in the semantic network (MacKay and Burke, 1990
; James, 2006
). The potential beneficial effects of tDCS would fit well with this framework as anodal stimulation decrease resting membrane potentials that in turn, could increase the likelihood of neuronal discharge in such a weakened network. Therefore, tDCS is mechanistically appealing as a rehabilitative tool for cognitive decline associated with healthy aging in addition to possible benefits in brain injured populations.
The choice of the ATLs as our stimulation site was motivated by a growing body of imaging literature suggesting this region as the location for representation of person-specific knowledge (Sergent et al., 1992
; Gorno-Tempini et al., 1998
; Leveroni et al., 2000
; Nakamura et al., 2000
; Gorno-Tempini and Price, 2001
; Grabowski et al., 2001
; Sugiura et al., 2001
; Pourtois et al., 2005
; Rotshtein et al., 2005
; Ross and Olson, 2010
) and neuropsychological data showing that focal lesions to the ATLs can cause multimodal person recognition deficits and impaired proper naming (Gainotti, 2007
; Olson et al., 2007
The observed tDCS effects on face naming in this study’s older sample was surprising because it was in the opposite hemisphere to what we observed in our younger sample. Left, more so than right, hemispheric stimulation led to a marked improvement in recall of face names relative to the sham condition. However, it should be pointed out that both left and right hemispheric stimulation led to improvements in both groups. The groups differed only in the dominance of this effect. Further, unlike in the younger sample, we observed that name recall of places was positively affected by right hemisphere anodal stimulation. This finding was unexpected, however there is some precedence for it in the literature given that ATL removal can at times cause proper name deficits for people as well as places (Tranel, 2009
We found that object naming and fluency as assessed in the BNT and Category fluency Test was related to person and landmark naming in our task. We hypothesized that beneficial effects of tDCS may be enhanced in older participants but found that the improvements in the elderly were comparable to those observed in the younger sample. Baseline language skills were not related to naming improvements during tDCS suggesting a more generalized benefit of stimulation in older adults.
It is important to note that one should be tentative in drawing inferences from tDCS effects about cortical functional organization. One reason is the limited spatial specificity of tDCS due to large electrode size and current spread such that its effects may influence a relatively wide area of potentially functionally heterogeneous cortex (Wagner et al., 2007
). Another reason is that depolarization and hyperpolarization of resting membrane potentials, and therefore the enhancing and inhibitory effects, depend on the orientation of neural cell populations relative to the current flow and the direction of the current (Nitsche and Paulus, 2000
). The cortical folding pattern represents an inconsistent geometry of cell orientations allowing different tDCS effects for functions that are located in close proximity to one another and is complicated by inter-subject variability in cortical folding.
While this study was explicitly designed to explore the rehabilitative utility of tDCS in age-associated naming deficits rather than to provide a detailed account of the functional specialization of the ATLs for proper name recall, we can at least speculate on possible reasons for the differences between tDCS effects in younger and older individuals, keeping the above caveats in mind. A common finding in the aging literature is evidence of functional reorganization reflected by a hemispheric asymmetry reduction in BOLD signal (Cabeza, 2002
; Dolcos et al., 2002
; Li et al., 2009
). The hemispheric asymmetry reduction in older adults (HAROLD) model poses that these changes reflect compensatory processes due to under- or inefficient recruitment of the specialized, unilateral networks activated in young adults. This compensatory recruitment is often in homologous regions in the contralateral hemisphere from the cortical regions activated in young adults. Furthermore, such compensatory behavior may be differentially instantiated dependent on task and subject related factors (Cabeza, 2002
; Park and Reuter-Lorenz, 2009
). It is possible that the observed effects here reflect promotion of this compensatory activity in the left ATL with anodal tDCS over this structure in support of ineffective unilateral right ATL recruitment, which underlies face naming in young adults. Direct right ATL stimulation, which produced a more modest, but not statistically significant benefit in the older adults, may be less effective in overcoming inherent inefficiencies than stimulation of alternative networks to support performance. Such a result is not without precedent as Sole-Padulles et al. (2006
) described a face–name episodic encoding task in which repetitive transcranial magnetic stimulation to the prefrontal cortex enhanced activity in this region and improved memory performance in older adults presumably by compensating for inefficient memory networks.
Another possible explanation for the observed differences is based on the different stimulus material used for young and older participants. In the young adults, knowledge of most of the famous faces was likely acquired relatively recently. In contrast, the knowledge about faces (and places) in our older sample was presumably learned decades ago (such as the face of Marilyn Monroe). The search for the name of a person that has been learned a long time ago may place different demands on the neural networks underlying name recall and may involve a more comprehensive search through long-term memory.
A different explanation for the observed differences between older and younger participants derives from the complexity of the processes underlying person recognition and proper naming. The access to phonological representations in a name recall task is thought to be a late step in a serial information processing hierarchy (Bruce and Young, 1986
; Burton et al., 1990
; Galdo Alvarez et al., 2009
). In our previous publication (Ross et al., 2010
) we speculated that the right-sided effects in younger adults were due to the modulation of right hemispheric neural networks underlying the recognition or retrieval of person-specific semantic information rather than the recall of its name. This idea is supported by studies of patients with focal ATL lesions that have shown that right-sided damage tends to be associated with the loss of feelings of familiarity and access to biographical information (excluding the name; Gainotti, 2007
; Gainotti et al., 2010
). In our experiment this enhanced ability for person recognition may in turn have affected the downstream retrieval of left-hemisphere phonological representations (Burton and Bruce, 1992
). It is possible that in older adults, tDCS enhanced this later stage which has been shown to have a left hemispheric focus (Tranel et al., 1997
; Grabowski et al., 2001
; Tranel and Jones, 2006
; Tsukiura et al., 2006
). Therefore, tDCS in the elderly would seem to have a most robust effect in situations similar to a true “tip of the tongue” state. Here, a person or object is already recognized and the recall of the proper name is subjectively perceived to be imminent but cannot be accessed (Maylor, 1990
; Burke et al., 1991
). It should be mentioned here that this phenomenon is often experienced with proper names, but is not necessarily limited to them. The significant relationship in our data between neuropsychological test performance in tasks involving object naming (BNT) and verbal fluency (Category fluency) and performance in our proper name task suggest that tDCS may be effective in language production in general. This is indeed supported by experiments investigating word and name retrieval in patients with aphasia (Monti et al., 2008
; Fiori et al., 2010
; Fridriksson et al., 2011
) and healthy participants (Fertonani et al., 2010
). The recall of proper names can be seen as a special case of name retrieval due to the unique and arbitrary nature of proper names that are often harder to access.
In conclusion, recall of proper names in older adults can be enhanced with electrical stimulation over the ATLs. Anodal tDCS improved proper naming of both famous faces and landmarks with left and right ATL stimulation, respectively. The effects of face naming observed here were of a similar magnitude to that of young adults, but only older adults demonstrated an effect on place naming, suggesting a potential more general benefit of anodal stimulation. Our data lend support to increasing evidence of the effectiveness of tDCS as a potential tool for the neurorehabilitation of cognitive function in healthy and pathological cognitive decline. However, more research is needed to clarify the exact conditions under which the applications of tDCS can be useful.