COGNITIVE NEUROSCIENCE
Selective processing of buildings and faces during
working memory: the role of the ventral striatum
Alexa Haeger,
1,2
Hweeling Lee,
2
Juergen Fell
1
and Nikolai Axmacher
2,3
1
Department of Epileptology, University of Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, Germany
2
German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany
3
Department of Neuropsychology, Institute of Cognitive Neuroscience, Ruhr-University Bochum, Universit€ atsstrasse 150, 44801
Bochum, Germany
Keywords: distraction, fMRI, interference resolution, striatum, working memory
Abstract
The ventral striatum seems to play an important role during working memory (WM) tasks when irrelevant information needs to be
filtered out. However, the concrete neural mechanisms underlying this process are still unknown. In this study, we investigated
these mechanisms in detail. Eighteen healthy human participants were presented with multiple items consisting of faces or build-
ings. They either had to maintain two or four items from one category (low- and high-memory-load condition), or two from one
category and suppress (filter out) two items from the other category (distraction condition). Striatal activity was increased in the
distraction as compared with the high-load condition. Activity in category-specific regions in the inferior temporal cortex [fusiform
face area (FFA) and parahippocampal place area (PPA)] was reduced when items from the other category needed to be selec-
tively maintained. Furthermore, functional connectivity analysis showed significant reduction of striatal–PPA correlations during
selective maintenance of faces. However, striatal–FFA connectivity was not reduced during maintenance of buildings vs. faces,
possibly because face stimuli are more salient. Taken together, our results suggest that the ventral striatum supports selective
WM maintenance by reduced gating of task-irrelevant activity via attenuating functional connectivity without increasing task-rele-
vant activity correspondingly.
Introduction
Working memory (WM) depends both on regions exerting control
functions and on areas supporting the perceptual representation of
the information that needs to be maintained (Baddeley et al., 1974).
During real-world situations, limited WM capacity requires one to
assign transient storage space to relevant pieces of information while
filtering out irrelevant ones. The basal ganglia, consisting of the stri-
atum (caudate nucleus and putamen), globus pallidus, nucleus ac-
cumbens and subthalamic nucleus, are implicated in such WM
processes (Owen et al., 1998; Packard & Knowlton, 2002; Cools,
2005; Frank, 2005; Baier et al., 2010). The striatum in particular is
hypothesized to act as a gateway for resolving interfering informa-
tion by increasing the likelihood of processing relevant information
whilst minimizing the influence of irrelevant information (Cools
et al., 2006; Dahlin et al., 2008; McNab & Klingberg, 2008; Frank
& Fossella, 2011; Badre & Frank, 2012; Scimeca & Badre, 2012).
This especially applies for novel items (e.g. Bunzeck & D€ uzel,
2006; Guitart-Masip et al., 2010). However, the exact mechanisms
by which the striatum supports interference resolution during WM
maintenance are still unknown.
Here, we investigated the role of the ventral striatum in filtering
of task-relevant and task-irrelevant complex representations of faces
and buildings during visual WM. Participants performed a modified
Sternberg WM task that manipulated target category (faces vs.
buildings) and WM load (low, distraction, high) while being
scanned. Faces predominantly induce activation in the fusiform gyri
[fusiform face area (FFA); Kanwisher et al., 1997, 1999; Maguire
et al., 2001], while buildings elicit selective responses in the para-
hippocampal gyri [parahippocampal place area (PPA); Epstein &
Kanwisher, 1998; Maguire et al., 2001]. Thus, we hypothesize that
during selective maintenance of one of the two target categories (i.e.
during the distraction condition), the striatum acts as a gateway to
resolve interfering information by modulating activity in the FFA
and PPA.
These hypotheses extend previous work in two aspects. First, we
investigated an issue that yielded controversial results in the existing
literature, namely whether the striatum facilitates activity in task-rel-
evant regions (Egner & Hirsch, 2005; Gruber et al., 2006), sup-
presses activity in task-irrelevant regions (Maier et al., 2008), or
both (Gazzaley et al., 2005; O’Reilly & Frank, 2006). We addressed
this open question by using a novel design. In contrast to previous
studies, we chose an experimental task that allowed us to compare
maintenance in the presence of distraction with maintenance when
only items from a single category were presented, which is impor-
tant to isolate distraction-related effects. Second, we examined the
Correspondence: Dr N. Axmacher,
3
Department of Neuropsychology, as above.
E-mail: nikolai.axmacher@ukb.uni-bonn.de
Received 8 August 2014, accepted 19 November 2014
© 2014 Federation of European Neuroscience Societies and John Wiley & Sons Ltd
European Journal of Neuroscience, Vol. 41, pp. 505–513, 2015 doi:10.1111/ejn.12808