Elsevier

Neuropsychologia

Volume 73, July 2015, Pages 176-194
Neuropsychologia

Parietal lesion effects on cued recall following pair associate learning

https://doi.org/10.1016/j.neuropsychologia.2015.05.009Get rights and content

Highlights

  • Investigated recollective role of ventral parietal cortex.

  • Lesion-effects study of cued recall following pair-associate learning.

  • Checked recall of word pairs, picture pairs, picture–sound pairs.

  • Area lesion extent–performance correlations and VLSM identified relevant areas.

  • Angular gyrus implicated in cued recall deficits, especially in cross-modal task.

Abstract

We investigated the involvement of the posterior parietal cortex in episodic memory in a lesion-effects study of cued recall following pair-associate learning. Groups of patients who had experienced first-incident stroke, generally in middle cerebral artery territory, and exhibited damage that included lateral posterior parietal regions, were tested within an early post-stroke time window. In three experiments, patients and matched healthy comparison groups executed repeated study and cued recall test blocks of pairs of words (Experiment 1), pairs of object pictures (Experiment 2), or pairs of object pictures and environmental sounds (Experiment 3). Patients' brain CT scans were subjected to quantitative analysis of lesion volumes. Behavioral and lesion data were used to compute correlations between area lesion extent and memory deficits, and to conduct voxel-based lesion-symptom mapping. These analyses implicated lateral ventral parietal cortex, especially the angular gyrus, in cued recall deficits, most pronouncedly in the cross-modal picture–sound pairs task, though significant parietal lesion effects were also found in the unimodal word pairs and picture pairs tasks. In contrast to an earlier study in which comparable parietal lesions did not cause deficits in item recognition, these results indicate that lateral posterior parietal areas make a substantive contribution to demanding forms of recollective retrieval as represented by cued recall, especially for complex associative representations.

Introduction

Identification of brain regions supporting mnemonic processes, and the interactions between those regions, has been the focus of much contemporary cognitive neuroscience research. Among the brain areas increasingly identified as playing a role in many forms of memory is the posterior parietal cortex. Although a host of electrophysiological and hemodynamic studies have reported prominent parietal activations during retrieval of episodic memory, the functional significance of such parietal activations is not yet clear. Suggestions regarding the contribution of parietal areas to memory include attentional functions (e.g. Cabeza, 2008; Cabeza et al., 2011; Ciaramelli et al., 2010, 2008), expectation and salience (Buchsbaum et al., 2011, Jaeger et al., 2013, O’Connor et al., 2010), retrieval buffering (e.g., Vilberg and Rugg, 2008, Vilberg and Rugg, 2009a, Vilberg and Rugg, 2009b), multimodal integration (e.g., Shimamura, 2011) and subjective aspects of remembering (e.g., Hower et al., 2014; Simons et al., 2010; reviewed by Levy (2012)).

The range of explanations of parietal mnemonic functions may be influenced by the types of memory tasks used to investigate them. Most parietal mnemonic imaging studies have used recognition memory tasks (e.g., Ciaramelli et al., 2010; Daselaar et al., 2006; Fleck et al., 2006; Kim and Cabeza, 2007, Kim and Cabeza, 2009; Wagner et al., 2005). Episodic recognition judgments are generally assumed to be supported by both familiarity and by recollection (Yonelinas, 2002). Several studies have linked dorsal parietal activations with recognition judgments based on familiarity, while ventral parietal cortex (VPC) activation has been associated with recollective processes, accompanied by retrieval of details related to the context of the experienced event (Cabeza, 2008, Cabeza et al., 2008, Cabeza et al., 2011). For example, VPC activation has been related to rich and vivid reliving of a prior experience (Frithsen and Miller, 2014, Kuhl and Chun, 2014), the subjective feeling of “oldness” (Wheeler and Buckner, 2003), and confidence in the oldness decision (Kim and Cabeza, 2007, Kim and Cabeza, 2009). Various assays have been used to determine the extent of the recollective contribution to recognition, such as subjective report (as in the Remember/Know paradigm; e.g., Duarte et al., 2008; Frithsen and Miller, 2014; Vilberg and Rugg, 2009a; Yonelinas et al., 2005) or success in binary decisions regarding source memory information (e.g., Donaldson et al., 2010; Frithsen and Miller, 2014).

While recall and recollection-based recognition are asserted to be supported by the same processes (e.g., Yonelinas, 2002), and this notion has received some empirical confirmation from neuroimaging (Okada et al., 2012, Schott et al., 2005), only a handful of studies have attempted to examine the mnemonic role of parietal cortices using recall measures, which arguably provide a more objective index of recollection. Kuhl and Chun (2014) examined parietal activations during a cued recall task, using multimodal word–face and word–scene pairs, for which the word served as a retrieval cue. However, they did not include an objective measure of recollection in their study (Trelle, 2014). A few studies (Hayama et al., 2012, Okada et al., 2012) have examined parietal activations during cued recall using word stem cues. While those studies provides a valuable additional perspective on retrieval, word stem cues arguably provide part of the retrieval target for inspection, and may not fully recruit recollective processes. Seibert and colleagues (Seibert et al., 2011, Seibert et al., 2011) examined cued recall for episodic encoding of picture pairs using MEG and fMRI, but assessed retrieval by examining performance on a living/non-living classification task performed on retrieved pair members compared with a control condition in which classification was done on presented stimuli. It was not determined whether retrieval was correct on a trial by trial basis. Therefore, those results reflect retrieval orientation more than retrieval success, and also might have included a relatively high percentage of guess-based responses.

Furthermore, while the hemodynamic studies mentioned above indicate that VPC activation is related to recollective aspects of recognition, they do not determine whether VPC integrity is necessary for successful episodic retrieval. The handful of neuropsychological studies which relate to this issue (some reviewed by Schoo et al. (2011)) suggest that parietal lobe damage may not impair recognition memory accuracy (Ally et al., 2008, Ciaramelli et al., 2010, Haramati et al., 2008).

Neuropsychological studies employing Remember/Know and source memory paradigms have shown that parietal lesions may have no effect on retrieval success, leading rather to reductions in subjective recollective experience (Berryhill et al., 2007, Davidson et al., 2008), reductions in confidence (Berryhill et al., 2009, Hower et al., 2014, Simons et al., 2010), increases in response time (Ciaramelli et al., 2010) or difficulty in the integration of memory cues (Dobbins et al., 2012).

Seemingly, additional neuropsychological studies are warranted to clarify whether VPC is integral to the recollective process. We therefore extended our earlier study of the effects of parietal lesions on recognition (Haramati et al., 2008) by examining lesion effects on cued recall. Specifically, we tested the effects of brain infarcts in middle cerebral artery (MCA) territory. Such infarcts are likely to yield damage to VPC components supramarginal gyrus and angular gyrus (but generally do not affect superior parietal lobes). We chose to examine recall in response to episodic cues following pair associate learning, which can only be accomplished by retrieval of cue-target episodic association, representing a strong expression of the recollective process. We tested recall following associative learning of several types of associative pairs: auditory word pairs, unimodal visual object pairs, and cross-modal object picture–object sound pairs.

If VPC is a necessary substrate of the recollective processes, lesions of that area should cause deficits in cued recall. Additionally, we reasoned that the parietal cortex might be especially important for the representation of cross-modal associations, in line with the CoBRA model (cortical binding of relational activity; Shimamura, 2011), which suggests that VPC (specifically the angular gyrus) enhances episodic binding of information from other cortical inputs (Mesulam, 1998, Shimamura, 2011). In contrast, the account that views VPC retrieval related activations as reflecting post-retrieval capture of attention by retrieved representations (e.g., Cabeza et al., 2011), and the expectation and salience accounts (Buchsbaum et al., 2011, O’Connor et al., 2010), which do not assign a causal recollective role to VPC, predict in principle that VPC damage would yield no cued recall deficits. Similarly, approaches which view the VPC contribution to retrieval primarily as related to subjective recollective experience (e.g., Ally et al., 2008; Simons et al., 2010; Yazar et al., 2014) would also generally predict that lesions should not impair objective cued recall performance.

Since damage-based deficits might be ameliorated as a result of compensatory reorganization (Schoo et al., 2011), to assess VPC lesion effects we tested patients within an early and narrow window of time after onset, after initial edemas subside, but before resolution of compensatory plasticity processes (Haramati et al., 2008). Since MCA territory stroke lesions are rarely limited strictly to parietal cortices, we employed voxel-based lesion-symptom mapping and area damage–performance correlations in order to determine the relative contributions of parietal and other cortical and subcortical regions to memory performance.

Section snippets

General patient group characteristics

The data of the current study were collected over the course of several years, and different numbers of patients took part in each of the three experiments reported below. All patients were recruited for the study and tested during their hospitalization at the Loewenstein Rehabilitation Hospital, Raanana, Israel, during the subacute period after the onset of stroke. All patients provided informed consent to participate in the study, which was performed using a protocol approved by the human

Patients

48 first incident stroke patients with lesions confirmed by semi-automatic analysis of computerized tomography (CT) scans (see below) as including posterior parietal damage, ages 26–82 years, participated in this study. Imaging data and clinical assessment indicated that 35 patients had right hemisphere damage (RHD); of these, 6 patients were left-handed and 14 were female. The RHD group mean age was 61.8 years (SD=13), and had a mean of 13.6 years of formal education (SD=3.3). 13 patients had

Patients

27 patients similar in their characteristics to those in Experiment 1 participated in Experiment 2. Patients' ages were 40–81 years. 19 patients had RHD; of those, 2 participants were left-handed and 5 were female. The RHD group mean age was 63.5 years (SD=10.1), and had a mean of 13.5 years of formal education (SD=3.4). 8 patients had LHD; of these, 1 was left-handed and 4 were female. The LHD group's mean age was 67.5 years (SD=8.0), and had a mean of 14.8 years of formal education (SD=4.0).

Patients

13 patients, aged 40–81 years, similar in their characteristics to the patients in the previous experiments participated in this study. 7 patients had RHD; 1 was left-handed and 1 was female. The RHD group’s mean age was 67.1 years (SD=13.5), and had a mean of 13.4 years of formal education (SD=3.0). 6 patients had LHD; 1 was left-handed and 3 were female. The LHD group's mean age was 68 years (SD=7.5), and had a mean of 15.7 years of formal education (SD=4.2). Table 1 details the demographic

Comparison group performance across tasks

One goal of the current study was to examine whether cortical lesions including the lateral parietal region differentially affect cued recall of unimodal verbal and visual and cross-modal audio–visual pair associate learning. In order to make that comparison most effectively, we attempted to create test conditions in which the fundamental difficulty of those memory tasks were as similar as possible, such that putative lesion effects could be best understood as reflecting qualitative differences

Discussion

In the current study, we attempted to assess the contribution of ventral parietal cortices to recollection by investigating lesion effects on three cued recall tasks, following the pair-associate learning of word pairs, picture pairs and picture–sound pairs. These tests revealed that groups of patients with MCA territory lesions exhibited differential degrees of impairment in the cued recall tasks relative to matched healthy controls. The least impairment was seen in cued recall of verbal pair

Acknowledgments

This work was supported by Israel Science Foundation grant 611/09 and German-Israeli Foundation for Scientific Research and Development grant 1083-5.4/2010 to DAL. We thank Roni Tibon, Nava Traschanski and Shahar Shefer for assistance with experimental design, data collection and analysis.

References (63)

  • L. Jacobson et al.

    Oppositional transcranial direct current stimulation (tDCS) of parietal substrates of attention during encoding modulates episodic memory

    Brain Res.

    (2012)
  • A. Jaeger et al.

    Unexpected novelty and familiarity orienting responses in lateral parietal cortex during recognition judgment

    Neuropsychologia

    (2013)
  • H. Kim et al.

    Common and specific brain regions in high- versus low-confidence recognition memory

    Brain Res.

    (2009)
  • S.M. Nelson et al.

    A parcellation scheme for human left lateral parietal cortex

    Neuron

    (2010)
  • D. Pergolizzi et al.

    Transcranial direct current stimulation (tDCS) of the parietal cortex leads to increased false recognition

    Neuropsychologia

    (2015)
  • M.D. Rugg et al.

    Brain networks underlying episodic memory retrieval

    Curr. Opin. Neurobiol.

    (2013)
  • T.M. Seibert et al.

    Parietal activity in episodic retrieval measured by fMRI and MEG

    NeuroImage

    (2011)
  • C. Sestieri et al.

    Interference with episodic memory retrieval following transcranial stimulation of the inferior but not the superior parietal lobule

    Neuropsychologia

    (2013)
  • J.S. Simons et al.

    Is the parietal lobe necessary for recollection in humans?

    Neuropsychologia

    (2008)
  • J. Solomon et al.

    User-friendly software for the analysis of brain lesions (ABLe)

    Comput. Methods Progr. Biomed.

    (2007)
  • N. Tzourio-Mazoyer et al.

    Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain

    NeuroImage

    (2002)
  • M.R. Uncapher et al.

    Roadmap to brain mapping: toward a functional map of human parietal cortex

    Neuron

    (2010)
  • K.L. Vilberg et al.

    Memory retrieval and the parietal cortex: a review of evidence from a dual-process perspective

    Neuropsychologia

    (2008)
  • K.L. Vilberg et al.

    An investigation of the effects of relative probability of old and new test items on the neural correlates of successful and unsuccessful source memory

    NeuroImage

    (2009)
  • A.D. Wagner et al.

    Parietal lobe contributions to episodic memory retrieval

    Trends Cogn. Sci.

    (2005)
  • A.P. Yonelinas

    The nature of recollection and familiarity: a review of 30 years of research

    J. Mem. Lang.

    (2002)
  • E. Bates et al.

    Voxel-based lesion-symptom mapping

    Nat. Neurosci.

    (2003)
  • M.E. Berryhill et al.

    Bilateral parietal cortex damage does not impair associative memory for paired stimuli

    Cogn. Neuropsychol.

    (2009)
  • M.E. Berryhill et al.

    Parietal lobe and episodic memory: Bilateral damage causes impaired free recall of autobiographical memory

    J. Neurosci.

    (2007)
  • B.R. Buchsbaum et al.

    Recency effects in the inferior parietal lobe during verbal recognition memory

    Front. Hum. Neurosci.

    (2011)
  • R. Cabeza et al.

    The parietal cortex and episodic memory: an attentional account

    Nat. Rev. Neurosci.

    (2008)
  • Cited by (48)

    • Lesion-behaviour mapping reveals multifactorial neurocognitive processes in recognition memory for unfamiliar faces

      2021, Neuropsychologia
      Citation Excerpt :

      There was no main effect of test phase, F(1,159) = 1.58, p = .21. As a result of the heterogeneity in patients’ age, which can affect memory performance, for the lesion-behavior analysis, we used the more individually focused age-matched Z score as the behavioral measure for each patient (for a similar method, see Ben-Zvi et al., 2015). Table S2 shows the extent of damage to each region of the AAL and WM atlases in each patient.

    • Deconstructing the Posterior Medial Episodic Network

      2020, Trends in Cognitive Sciences
      Citation Excerpt :

      The Contextual Integration Model [84] proposes that AG maintains an integrated sensory representation of contextual details, such as colors and emotions, that, when integrated with foundational what-when-where details reactivated by hippocampus, can enhance a sense of vivid recollection. In support, research has demonstrated involvement of AG in more qualitative aspects of memory beyond hippocampal relational binding, including confidence and vividness of remembering [89–91], forming an egocentric perspective during recollection [92], recall of multimodal associations [27,93,94], and the precision of episodic recall [22,25,95]. Although these ideas focus specifically on AG, what is observed in AG is often reflected in the other cortical regions of the PM network [85].

    View all citing articles on Scopus
    View full text