Elsevier

Brain and Cognition

Volume 113, April 2017, Pages 32-39
Brain and Cognition

Non-invasive brain stimulation targeting the right fusiform gyrus selectively increases working memory for faces

https://doi.org/10.1016/j.bandc.2017.01.006Get rights and content

Highlights

  • Anodal tDCS was administered to right fusiform gyrus.

  • Participants performed a variable load working memory task with face/house stimuli.

  • Anodal tDCS enhanced face but not house memory performance.

  • Working memory capacity predicted influence of tDCS.

Abstract

The human extrastriate cortex contains a region critically involved in face detection and memory, the right fusiform gyrus. The present study evaluated whether transcranial direct current stimulation (tDCS) targeting this anatomical region would selectively influence memory for faces versus non-face objects (houses). Anodal tDCS targeted the right fusiform gyrus (Brodmann’s Area 37), with the anode at electrode site PO10, and cathode at FP2. Two stimulation conditions were compared in a repeated-measures design: 0.5 mA versus 1.5 mA intensity; a separate control group received no stimulation. Participants completed a working memory task for face and house stimuli, varying in memory load from 1 to 4 items. Individual differences measures assessed trait-based differences in facial recognition skills. Results showed 1.5 mA intensity stimulation (versus 0.5 mA and control) increased performance at high memory loads, but only with faces. Lower overall working memory capacity predicted a positive impact of tDCS. Results provide support for the notion of functional specialization of the right fusiform regions for maintaining face (but not non-face object) stimuli in working memory, and further suggest that low intensity electrical stimulation of this region may enhance demanding face working memory performance particularly in those with relatively poor baseline working memory skills.

Introduction

The ability to detect and remember faces is critical to human social functioning, allowing us to know when people are present, recognize a familiar face, and identify known individuals (Kanwisher & Yovel, 2006). These processes involve a network of interrelated brain regions including at least the inferior occipital gyrus, superior temporal sulcus, and lateral fusiform gyrus (Haxby, Hoffman, & Gobbini, 2002). The most consistently implicated region in this network is the right fusiform gyrus, a portion of which has been termed the “fusiform face area” (FFA) by Kanwisher and colleagues (Kanwisher, McDermott, & Chun, 1997). Though subject to debate (Gauthier et al., 1999, Kanwisher and Yovel, 2006) this region is thought to serve as a specialized module for face perception, responding maximally to the perception of face stimuli relative to non-face objects such as houses (Haxby et al., 1999), cars (Grill-Spector, Knouf, & Kanwisher, 2004), or flowers (McCarthy, Puce, Gore, & Allison, 1997).

One popular method for examining the specialized ability for individuals to process and maintain faces is to engage them in a working memory task with varying load (e.g., maintaining 1–4 faces), and varying stimulus domains (e.g., maintaining faces versus houses) (Druzgal and D’Esposito, 2001, Druzgal and D’Esposito, 2003, Gazzaley et al., 2004, Ranganath et al., 2004). Overall, research has demonstrated parametrically increasing right fusiform gyrus activity (with fMRI) as working memory set size increases from 1 to 4 faces (Druzgal & D’Esposito, 2003), and much greater responses in this region to faces than houses (Yovel & Kanwisher, 2004). Thus, the right fusiform gyrus appears to be involved in the processing and maintenance of faces during a working memory task. Transcranial direct current stimulation (tDCS) provides a unique opportunity to explore causal relationships between right fusiform gyrus activity and working memory for faces, by selectively modulating brain activity in this region and measuring the impact the processing and maintenance of faces versus non-face objects.

Transcranial direct current stimulation (tDCS) involves non-invasively applying low intensity electrical current to brain regions by way of electrodes positioned on the surface of the scalp (Brunoni et al., 2012). In most studies, between 1.0 and 2.0 mA intensity direct current (DC) is administered by positioning electrodes in a manner intended to target brain regions of interest with anodal or cathodal polarity stimulation (Jacobson, Koslowsky, & Lavidor, 2012). A unidirectional flow of charge emanates from a single anode, propagates through cortical tissue, and returns via a single cathode; as anodal current propagates through the cortex, it produces neuronal membrane depolarization (Purpura & McMurtry, 1965), increases neuronal firing rates (Nitsche and Paulus, 2000, Nitsche and Paulus, 2001), and increases functional brain connectivity in task-related networks (Peña-Gómez et al., 2012). Though tDCS has been used extensively in the behavioral, cognitive, clinical, and affective sciences literature (Jacobson et al., 2012, Price et al., 2015, Shiozawa et al., 2014), very few studies have examined its influence on face processing or memory. In two of them, anodal tDCS was applied over the dorsolateral prefrontal cortex (Lafontaine, Theoret, Gosselin, & Lippe, 2013) or occipito-temporal cortex (which includes the FFA, the occipital face area (OFA), and superior temporal sulcus (Yang et al., 2014)), and outcomes were measured via event-related potentials (ERPs). In the first experiment, the authors found enhanced N170 repetition suppression, indicating faster face recognition with right hemisphere anodal stimulation. In the second experiment, the authors found anodal or cathodal stimulation to influence the N170 waveform during a face orientation task, an effect maximal over the right hemisphere. In a more recent study, Renzi and colleagues (Renzi et al., 2015) used anodal OFA stimulation and found reduced performance on a task involving the detection and discrimination of faces and non-face objects; right fusiform gyrus stimulation was not examined (see also (Barbieri, Negrini, Nitsche, & Rivolta, 2015)). Thus, existing research regarding putative tDCS influences on face processing and memory is equivocal, using varied stimulation targets and outcome measures, and finding mixed results.

Though tDCS has not yet been applied in the context of working memory for face stimuli, or for specifically targeting the right fusiform gyrus, an extensive literature examines the impact of tDCS on working memory task performance. Indeed one of the most reliable results in the tDCS literature is an enhancement of verbal n-back task performance with tDCS targeting the left dorsolateral prefrontal cortex (DLPFC) (Berryhill et al., 2014, Brunoni and Vanderhasselt, 2014). For instance, Ohn and colleagues found higher accuracy on a verbal n-back task with anodal versus sham tDCS targeting the left DLPFC, and Mulquiney and colleagues found faster response times on a verbal n-back task with anodal versus sham tDCS targeting the left DLPFC. This pattern is largely restricted to letter, digit, and word stimuli, though it is generally attributed to this brain region’s involvement in implementing attentional control strategies during working memory tasks (Callicott et al., 1999).

The present study was designed to build upon extant studies in four primary ways. First, we attempted to selectively target the right fusiform gyrus using algorithms that predict tDCS current propagation through cortical structures; no other studies have targeted this region in this manner. Though imperfect, these models afford some prediction of maximal focality and intensity at targeted brain structures (Datta et al., 2009, Dmochowski et al., 2011). Second, we used outcome measures that allow understanding tDCS influences on both face and non-face object working memory. Specifically, we adopted a task involving the delayed recognition of both faces and houses (Yovel & Kanwisher, 2004) with varied working memory load (i.e., set size). Previous fMRI research shows parametrically increasing right fusiform gyrus activity as face set size increases from 1 to 4 faces (Druzgal & D’Esposito, 2003), and much greater responses in this region to faces than houses (Yovel & Kanwisher, 2004). This research suggests that tDCS targeting this region may selectively impact face, but not house working memory, and that any tDCS impacts on face working memory may be load-contingent. If so, such results would provide unique causal evidence for the stimulus-specific and load-contingent role of the right fusiform gyrus during working memory tasks demanding the processing and maintenance of faces.

Third, we used individual differences measures to evaluate whether trait face recognition skills might predict the magnitude of our effects; recent studies suggest that individual differences can be valuable in understanding sometimes unreliable tDCS influences on perception and cognition (Berryhill and Jones, 2012, Brunyé, 2015, Brunyé et al., 2014, Jones et al., 2015, Slaby et al., 2015). Understanding baseline individual skills on domain-general (e.g., working memory) and domain-specific (e.g., face processing) tasks can provide predictive value for the impact of tDCS. For instance, recent research shows that tDCS of right medial temporal lobe regions only improves navigation performance for individuals with relatively poor spatial sense of direction (Brunyé, Holmes, et al., 2014), and tDCS of DLPFC only improved arithmetic performance for individuals with high mathematics anxiety (Sarkar, Dowker, & Cohen Kadosh, 2014). It is unknown how individual differences in working memory ability may modulate the influence of tDCS on face working memory task performance. Finally, we incorporate a mixed experimental design that controls for perceived cutaneous sensation and reduces the potential for experimental demand characteristics influencing arousal and task performance (Brunyé, Cantelon, Holmes, Taylor, & Mahoney, 2014).

While performing the working memory task (i.e., online), participants received either 0.5 mA or 1.5 mA active anodal tDCS, in a repeated-measures (crossover) design. We chose this design based on a review of recent literature. First, there is compelling evidence that online stimulation influences cognitive task performance either similarly to (Axelrod et al., 2015, Wirth et al., 2011), or more than (Martin, Liu, Alonzo, Green, & Loo, 2014), offline tDCS. Second, an anodal-excitatory effect is reliably obtained in cognitive literature (Jacobson et al., 2012), and we chose 1.5 mA because it reliably influences cortical excitability (Dymond, Coger, & Serafetinides, 1975) and cognitive task performance (Ditye et al., 2012, Javadi et al., 2012); furthermore, the influence of tDCS does not necessarily scale with increased intensity to 2.0 mA (Batsikadze, Moliadze, Paulus, Kuo, & Nitsche, 2013). Finally, we chose to use a low intensity stimulation control condition (0.5 mA) rather than sham due to recent research demonstrating cutaneous sensation differences in sham versus active stimulation conditions, and unintentional participant awareness of condition-based differences (Brunyé, Cantelon, et al., 2014). A 0.5 mA low intensity control condition reduces otherwise large differences in perceived sensation between active and sham conditions, without influencing cognitive task performance relative to sham (Brunyé et al., 2014, Nitsche and Paulus, 2000). In fact, to our knowledge only one sleep-related study suggests an influence of 0.5 mA stimulation on any cognitive, behavioral, or physiological measures (Marshall, Mölle, Hallschmid, & Born, 2004). To ensure no discernable influence of 0.5 mA stimulation on task performance, we also collected control data from a separate group of participants who received no stimulation.

We expect that tDCS targeting the right fusiform gyrus will influence performance on the working memory task; given the putative face-selective role of this region, we also expected this effect to be specific to faces, and not extend to houses. This effect may also emerge only at relatively high memory set sizes, given possible ceiling performance at low memory loads (Druzgal & D’Esposito, 2003), parametric increases in right fusiform gyrus activation with increasing memory loads (Druzgal & D’Esposito, 2003), and literature demonstrating a more reliable impact of tDCS on relatively difficult working memory tasks (Berryhill et al., 2014). It could also be the case that higher working memory loads with category-specific face stimuli necessitate increased engagement of the fusiform gyrus, whereas category-general working memory stimuli may not. If so, then we might also expect that individuals with relatively poor performance at high face memory loads may stand to benefit most from stimulation. For individual differences, no particular hypotheses were made with regard to tDCS influences, though we did expect that individuals with higher trait face recognition skills (Duchaine & Nakayama, 2006) would also demonstrate higher performance on the delay-recognition task. It could also be the case that high or low trait face recognition skills would produce ceiling or floor effects on our task, respectively, reducing any particular influence of tDCS.

Section snippets

Participants

Twenty-four healthy subjects participated (15 female, 9 male, age 21.3 ± 3.3) in the main experiment for monetary compensation. An additional 24 healthy subjects formed the control group to gain baseline data on the working memory task (17 female, 7 male, age 19.6 ± 3.6). Participants were randomly assigned to the main experimental versus control groups. Written informed consent was provided, in accordance with approvals by the Tufts University Institutional Review Board and U.S. Army Human

Results

Table 1 details mean and standard deviation Cowan’s K, hit rates, false alarm rates, sensitivity (d-prime), response criterion, and response times, for all conditions and groups.

Discussion

The present study examined whether low current electrical stimulation targeting the right fusiform gyrus would differentially influence performance on a variable load working memory task using face- versus house-based stimuli. We specifically compared 1.5 mA stimulation to a 0.5 mA stimulation condition (within-participants), and to a no stimulation control group (between-participants). Both within- and between-participants comparisons demonstrated that 1.5 mA stimulation increases the number of

Author contributions

T.T.B. and J.M.M. planned and designed the experiment. A.H. recruited and ran participants, and processed data. T.T.B. prepared the manuscript, and J.M.M., C.R.M., and H.A.T. provided critical manuscript revisions.

Acknowledgements

This work was supported by a grant awarded to H.A.T. from the U.S. Army Natick Soldier Research, Development, and Engineering Center (W911QY-13-C-0012). Permission was granted by the U.S. Army to publish this material. The views expressed in this article are solely those of the authors and do not reflect the official policies or positions of the Department of the Army, the Department of Defense, or any other department or agency of the U.S. government. The authors have no conflicts of interest

References (59)

  • J.V. Haxby et al.

    The effect of face inversion on activity in human neural systems for face and object perception

    Neuron

    (1999)
  • A.H. Javadi et al.

    Short duration transcranial direct current stimulation (tDCS) modulates verbal memory

    Brain Stimulation

    (2012)
  • K.T. Jones et al.

    The strategy and motivational influences on the beneficial effect of neurostimulation: A tDCS and fNIRS study

    NeuroImage

    (2015)
  • K. Monte-Silva et al.

    Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation

    Brain Stimulation

    (2013)
  • J.W. Peirce

    PsychoPy – Psychophysics software in Python

    Journal of Neuroscience Methods

    (2007)
  • C. Peña-Gómez et al.

    Modulation of large-scale brain networks by transcranial direct current stimulation evidenced by resting-state functional MRI

    Brain Stimulation

    (2012)
  • A.R. Price et al.

    A meta-analysis of transcranial direct current stimulation studies examining the reliability of effects on language measures

    Brain Stimulation

    (2015)
  • C. Ranganath et al.

    Category-specific modulation of inferior temporal activity during working memory encoding and maintenance

    Cognitive Brain Research

    (2004)
  • B. Rossion et al.

    Early lateralization and orientation tuning for face, word, and object processing in the visual cortex

    NeuroImage

    (2003)
  • M. Wirth et al.

    Effects of transcranial direct current stimulation (tDCS) on behaviour and electrophysiology of language production

    Neuropsychologia

    (2011)
  • G. Yovel et al.

    Face perception: Domain specific, not process specific

    Neuron

    (2004)
  • G. Avidan et al.

    Detailed exploration of face-related processing in congenital prosopagnosia: 2. Functional neuroimaging findings

    Journal of Cognitive Neuroscience

    (2005)
  • V. Axelrod et al.

    Increasing propensity to mind-wander with transcranial direct current stimulation

    Proceedings of the National Academy of Sciences

    (2015)
  • M. Barbieri et al.

    Anodal-tDCS over the human right occipital cortex enhances the perception and memory of both faces and objects

    Neuropsychologia

    (2015)
  • G. Batsikadze et al.

    Partially non-linear stimulation intensity-dependent effects of direct current stimulation on motor cortex excitability in humans

    The Journal of Physiology

    (2013)
  • M. Behrmann et al.

    Bilateral hemispheric processing of words and faces: Evidence from word impairments in prosopagnosia and face impairments in pure alexia

    Cerebral Cortex

    (2014)
  • M.E. Berryhill et al.

    Hits and misses: Leveraging tDCS to advance cognitive research

    Frontiers in Psychology

    (2014)
  • T.T. Brunyé

    Increasing breadth of semantic associations with left frontopolar direct current brain stimulation: A role for individual differences

    NeuroReport

    (2015)
  • T.T. Brunyé et al.

    Direct current brain stimulation enhances navigation efficiency in individuals with low sense of direction

    NeuroReport

    (2014)
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