Interference with episodic memory retrieval following transcranial stimulation of the inferior but not the superior parietal lobule
Highlights
► We examined the causal effect of repetitive TMS delivered at left parietal sites on episodic retrieval. ► A decrease of sensitivity for item recognition was observed for AG compared to SPL stimulation. ► A change in the criterion of source memory was observed for AG compared to SPL and sham stimulation. ► Inferior parietal lobule has a causal role in episodic retrieval. ► AG stimulation may have affected the weighing of the retrieved information for source attribution.
Introduction
The observation that left posterior parietal cortex (LPPC) is typically activated by episodic memory retrieval in human fMRI studies has generated many hypotheses concerning its role in the retrieval process (Cabeza et al., 2008, Vilberg and Rugg, 2008, Wagner et al., 2005). However, the validity of these theories is complicated by two factors: the correlational nature of fMRI, which precludes any firm conclusion about causal relationships between brain activity and cognitive functions, and the observation that lesions of PPC are commonly associated with visuo-spatial attention rather than memory deficits (Corbetta and Shulman, 2011, Mesulam, 1999).
Recent neuropsychological investigations have revealed that parietal patients do show subtle memory deficits that can go unnoticed during standard neuropsychological evaluations. Specifically, patients tend to have problems with subjective (e.g., less vividness/richness; less confidence, reduced sense of recollection) rather than objective (accuracy) aspects of recollection (Berryhill et al., 2007, Davidson et al., 2008, Simons et al., 2008, Simons et al., 2010). These clinical observations, however, appear quite modest if compared with the robust activation of LPPC in fMRI studies on healthy subjects, which would predict a more significant memory disruption. This apparent inconsistency may be explained by methodological differences across studies. Lesion studies have typically involved few patients with lesions of different size, location and degree of white matter damage, and the resulting inter-subject variability may have considerably weakened the possibility to isolate more objective memory deficits in these patients. This issue appears crucial when considering the high functional heterogeneity of this portion of cortex (Nelson et al., 2010, Sestieri et al., 2011). In addition, since most of the lesion studies have been conducted 6 months or more after the injury, the degree of functional reorganization in these patients is unknown (Schoo et al., 2011).
Transcranial magnetic stimulation (TMS) studies offer a potential solution to these problems, as this method can produce transient behavioral deficits that are thought to be associated with the function of the stimulated cortex or connected regions. The present rTMS study was designed to address several outstanding issues concerning the causal relationship between left parietal cortex and episodic retrieval.
First, it is currently unknown whether rTMS stimulation of LPPC produces deficits in paradigms assessing source memory, i.e., the memory for specific details of the context in which an item or event was previously encountered (Johnson, Hashtroudi, & Lindsay, 1993 for a review). Whereas item recognition memory is generally considered to depend on contributions from both recollection and familiarity (Yonelinas & Levy, 2002), source memory is considered a better test of recollection because success requires retrieval of the encoding context (Simons et al., 2008). The neuroimaging literature indicates that regions of the LPPC, and especially of the IPL, show stronger BOLD response for recollection, compared to familiarity (Cabeza et al., 2008, Vilberg and Rugg, 2008, Wagner et al., 2005). This may explain why previous rTMS studies (Manenti et al., 2010, Rossi et al., 2006), which have used item recognition paradigms, have failed to reveal memory deficits comparable to those observed during stimulation of the prefrontal cortex (Manenti et al., 2010, Rossi et al., 2001, Wais et al., 2011).
Second, neuropsychological studies (i.e., (Simons et al., 2010)) suggest that rTMS stimulation may selectively affect subjective measures of memory performance. Whereas objective measures assess performance in terms of accuracy (sensitivity) and speed (reaction times), subjective measures reflect, for example, how participants evaluate their performance (confidence), or what criterion (bias) they adopt during both old/new and taskA/taskB source memory decisions. For instance, during item recognition, subjects can differently weigh information about familiarity or recollection to indicate that they have seen an item before. In a similar vein, during source monitoring, subjects may have a bias toward a particular source category (criterion shift) because they weigh more one kind of information over another (e.g., semantic vs. visual) when attributing a memory detail to a particular source (Johnson et al., 1993).
A final issue concerns the spatial specificity of the potential rTMS effects. Consistent with previous studies (reviewed in (Vilberg and Rugg, 2008, Wagner et al., 2005), we have recently shown (Sestieri, Shulman, & Corbetta, 2010) that search for relevant information in episodic memory evokes significant BOLD responses in posterior nodes of the default mode network (DMN) (Raichle et al., 2001, Shulman et al., 1997), especially in the left angular gyrus (AG). We also reported the existence of a dynamic competition between this set of regions and an other set of parietal regions, included in the dorsal attention network (DAN), which are involved in perceptual search (SPL, posterior intraparietal sulcus). Importantly, this push–pull relationship was related to behavioral performance, as better performance at one task was associated with both greater BOLD activation in the set of task specific regions and greater deactivation in the other set of regions (Sestieri et al., 2010). This finding may reflect the existence of a mechanism of mutual suppression between functionally specialized parietal regions, based on task demands.
The present study aimed at fully characterizing the pattern of behavioral effects induced by rTMS interference on LPPC activity during a memory task that assessed both objective and subjective measures of item recognition and source memory using signal detection theory (SDT, (Green & Swets, 1966)). In order to increase the topographic precision of our rTMS procedure, we targeted specific sub-regions within LPPC. The first region (AG) has been shown to be specifically involved in searching for task-relevant information in episodic memory (Sestieri et al., 2010). To assess the topographic specificity of potential memory effects following AG stimulation, we also selected a region (SPL) that has been shown to be involved in perceptual search. Because previous fMRI have mainly reported left-lateralized parietal activations during memory retrieval (Wagner et al., 2005), we focused our investigation on stimulation sites in the left hemisphere.
Section snippets
Subjects
Sixteen right-handed (Oldfield, 1971) volunteers (age range: 20–38 years old; seven males) with normal or corrected to normal vision and no previous psychiatric or neurological history participated in the experiment. The experiment was conducted in accordance with the Code of Ethics of the World Medical Association, and with standards of the University of Chieti Institutional Review Board and Ethics Committee.
Experimental paradigm
Fig. 1 illustrates the TMS sites (A) and the experimental design ((B) and (C)). The
Results
Fig. 2 illustrates item recognition performance. The 1-way ANOVA revealed no effect of Condition on sensitivity [F(2,30)=1.25, p=n.s.] (Fig. 2A). However, it is interesting to note that item recognition performance during SHAM stimulation (d′=1.37) lied in between the performance observed during AG (d′=1.25) and SPL (d′=1.43) stimulation, potentially consistent with the presence of a competitive relationship between the two active sites. As a matter of fact, when directly comparing performance
Discussion
In the present study, we compared the effects of rTMS delivered to the inferior (AG) and superior (SPL) parietal lobule with a sham stimulation during an episodic memory retrieval task. Since different paradigm and measures of performance have been used in previous fMRI (reviewed in (Cabeza et al., 2008; Vilberg & Rugg, 2008; Wagner et al., 2005)), TMS (i.e., (Manenti et al., 2010; Rossi et al., 2006)) and lesion studies (e.g., (Berryhill et al., 2007; Davidson et al., 2008; Simons et al., 2008
Acknowledgments
This work was supported by the European Community’s Seventh Framework Programme (FP7/2007-2013), Grant Agreement ‘BrainSynch’ no. HEALTH-F2-2008-200728. We are grateful to Pasquale Cardellicchio, Ettore Ambrosini and Francesco DePasquale for technical help.
References (49)
- et al.
Does lateral parietal cortex support episodic memory? Evidence from focal lesion patients
Neuropsychologia
(2008) - et al.
The posterior parietal cortex in recognition memory: a neuropsychological study
Neuropsychologia
(2008) - et al.
Safety of rTMS to non-motor cortical areas in healthy participants and patients
Clinical Neurophysiology
(2006) - et al.
A parcellation scheme for human left lateral parietal cortex
Neuron
(2010) The assessment and analysis of handedness: the Edinburgh inventory
Neuropsychologia
(1971)- et al.
Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research
Clinical Neurophysiology
(2009) - et al.
Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee
Electroencephalography and Clinical Neurophysiology
(1994) - et al.
Is the parietal lobe necessary for recollection in humans?
Neuropsychologia
(2008) A population-average, landmark- and surface-based (PALS) atlas of human cerebral cortex
Neuroimage
(2005)- et al.
Memory retrieval and the parietal cortex: a review of evidence from a dual-process perspective
Neuropsychologia
(2008)
Parietal lobe contributions to episodic memory retrieval
Trends in Cognitive Sciences
Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the international workshop on the safety of repetitive transcranial magnetic stimulation, June 5–7, 1996
Electroencephalography and Clinical Neurophysiology
Inference on means using the bootstrap
Annals of Statistics
Parietal lobe and episodic memory: bilateral damage causes impaired free recall of autobiographical memory
Journal of Neuroscience
Visual long-term memory has a massive storage capacity for object details
Proceedings of the National academy of Sciences of the United States of America
The parietal cortex and episodic memory: an attentional account
Nature Reviews Neuroscience
Frontoparietal cortex controls spatial attention through modulation of anticipatory alpha rhythms
Journal of Neuroscience
Differential contribution of right and left parietal cortex to the control of spatial attention: a simultaneous EEG-rTMS study
Cerebral Cortex
Spatial neglect and attention networks
Annual Review of Neuroscience
Levels of processing: past, present and future?
Memory
A review of bootstrap confidence intervals
Journal of the Royal Statistical Society: Series B
True memory, false memory, and subjective recollection deficits after focal parietal lobe lesions
Neuropsychology
Effects of unilateral prefrontal lesions on familiarity, recollection, and source memory
Journal of Neuroscience
An introduction to the bootstrap
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2019, NeuropsychologiaCitation Excerpt :In the young group it would appear that left parietal cortex is vital – for example the area of supramarginal gyrus indicted in our classification analysis - whereas in the older group we revealed evidence of a wider network, which encompasses the angular gyrus in both hemispheres. The involvement of angular gyri in our task harmonises with evidence from previous neuropsychological, neural disruption and functional imaging studies that these regions are involved with the subjective experience of recalling an episodic memory (eg., Davidson et al., 2008; Sestieri et al., 2013; Marcotti and St Jacques, 2018). We suggest that recall of our memory from an egocentric perspective – as we experienced it at the time – is crucial to this sense of subjective experience.