Elsevier

NeuroImage

Volume 189, 1 April 2019, Pages 589-600
NeuroImage

Choice-predictive activity in parietal cortex during source memory decisions

https://doi.org/10.1016/j.neuroimage.2019.01.071Get rights and content

Highlights

  • BOLD activity in parietal cortex scales with evidence for source memory decisions.

  • Choice-predictive activity increases as a function of decision evidence.

  • Choice-predictive patterns in the parietal lobe are shared across subjects.

  • Multivariate activity in lateral parietal and medial temporal regions is correlated.

  • Activity in lateral parietal regions appears to reflect a decision variable.

Abstract

Neurobiological research has classically focused on perceptual decision-making, although many real-life decisions are based on information that is not currently available but stored in long-term memory. Previous studies have suggested that the lateral parietal cortex encodes decision-related signals during item recognition judgments. In the present fMRI study, we employed a parametric manipulation of evidence for source memory judgments and tested several hypotheses concerning memory decision signals in parietal cortex. As expected, the mean BOLD signal in several parietal regions was modulated by decision evidence. An analysis of the locally distributed pattern of activity, moreover, identified a parietal cluster showing significant choice-predictive activity even at the lowest level of decision evidence, with decoding accuracy that increased as a function of evidence. Decoding patterns were consistent across subjects as shown by a leave-one-subject-out classification analysis. Finally, we found that the pattern of choice-predictive activity in parietal lobe was temporally correlated with that observed in medial temporal regions traditionally associated with long-term memory functions. The present findings are consistent with a general role of lateral parietal regions located around the intraparietal sulcus in representing a decision variable for memory-based decisions.

Introduction

Research on the neural mechanisms supporting decision-making in humans and primates has primarily focused on perceptual decisions. However, many real-life decisions are also based on information stored in long-term memory (Sestieri et al., 2017; Shadlen and Kiani, 2013). Choosing a particular restaurant based on our previous experience is an example of how episodic memory informs decision-making. The interest on the neural signals underlying memory-based decisions originated from the observation that activity in lateral parietal cortex appears to reflect the subjective, rather than the objective, memory status (seen vs. unseen) of an item (Kahn et al., 2004; Wheeler and Buckner, 2003), as if activity in this region were determining the outcome of the memory judgment. In line with influential neurobiological models of perceptual decisions, the “mnemonic accumulator” hypothesis (Wagner et al., 2005) have proposed that parietal activity during memory retrieval reflects the neural implementation of a diffusion process, in which decision evidence is accumulated over time from a starting point to a decision bound (Ratcliff, 1978; Smith and Ratcliff, 2004). Consistent with the hypothesis, we have recently shown that the activity in a parietal area follows the parametric manipulation of evidence for old decisions during old/new recognition judgments (Sestieri et al., 2014). According to a recent model (Sestieri et al., 2017), this area belongs to a series of regions located along the intraparietal sulcus that contribute to memory-based decision-making and manipulation of retrieved information, and differs from more ventral and posterior parietal regions associated with the representation of retrieved information.

Despite the mounting evidence for the involvement of the lateral parietal cortex in item recognition decisions, there are still several outstanding issues concerning the neural bases of memory-based decision-making. A first question concerns the role of lateral parietal regions in representing a decision variable during other forms of memory decisions, such as those involving the evaluation of specific aspects of the encoding context (Mitchell and Johnson, 2009). The neuropsychological literature has classically associated deficits of source memory with lesions of medial temporal (Mayes et al., 2007) and frontal (Janowsky et al., 1989) cortices, but neuroimaging studies have frequently reported the involvement of the parietal lobe in source monitoring tasks (reviewed in (Mitchell and Johnson, 2009)). In the present study we tested whether all, or a subset, of these regions track decision evidence, defined as the amount of information favoring one of two possible alternatives, also for source memory decisions.

Secondly, despite the manipulation of stimulus difficulty is often used to identify decision-related activity in perceptual studies (Heekeren et al., 2008), the effect of decision evidence in source memory tasks could be also interpreted on the basis of other accounts, e.g. differential amount of retrieved information (Guerin and Miller, 2011). Thus, the decision-making account must be supported by an additional index of decision-related activity that is not solely based on the amount of decision evidence, such as the demonstration of choice-predictive locally distributed signals (Hebart et al., 2012; Rissman and Wagner, 2012). Specifically, regions that represent a decision variable should exhibit choice-predictive activity also in the most difficult condition, which is characterized by many source misattributions, and scale with the level of evidence for the source memory decision, reflecting the increasing difference in the local spatial distribution of activity for the two outcomes. In this respect, our approach differs considerably from previous studies that demonstrated successful decoding of memory content in parietal areas (Bonnici et al., 2016; Kuhl and Chun, 2014; Xiao et al., 2017). In particular, these studies required the recall of specific information associated with a particular cue, with no forced choice between two alternatives, and focused on the reactivation of the encoding pattern during recall, likely emphasizing the contribution of regions associated with the representation of retrieved information.

Thirdly, recent findings suggest that the spatial distribution of retrieval-related activity in high-level cortical areas is similar across subjects (Chen et al., 2017; Kragel and Polyn, 2016; Richter et al., 2016; Rissman et al., 2010), but so far there is no evidence that choice-predictive signals tracking decision evidence show a similar spatial organization across subjects. Significant across-subject decoding would not only demonstrate the spatial consistency of choice-predictive voxels but also imply a similar representation of memory choices across individuals. Finally, according to the mnemonic accumulator hypothesis, regions involved in the representation of memory decision variables should read/integrate mnemonic information from regions of the medial temporal lobe (MTL) traditionally associated with memory retrieval (Squire, 1992). This communication should be supported by a significant inter-regional interaction. However, evidence for such MTL-parietal functional coupling during memory decision-making is scarce (Cabeza et al., 2011; Geib et al., 2017; Kuhl et al., 2013).

To address these issues, we used univariate and multivariate analyses of fMRI activity during a source memory task that involved the manipulation of the amount of evidence for deciding whether an object image had been previously encoded together with face or place images. This was obtained through the manipulation of study repetitions, i.e. the number of stimulus exposures in the encoding phase, based on the assumption that the number of study repetitions provides graded evidence for a source memory decision (in analogy with the effect of sensory evidence, i.e., motion coherence, for motion direction discrimination in perceptual decisions (Gold and Shadlen, 2007).

Section snippets

Subjects

Participants gave informed consent in accordance with guidelines set by the Human Studies Committee of G. D'Annunzio Chieti University (protocol #1007, approved on March 18th, 2016). Nineteen healthy right-handed subjects (10 males, mean age 25 ± 3 years) participated in the study. One subject was excluded from the analysis because his behavioral performance was at chance level. The study included a behavioral encoding session in the morning (duration: approx. 1 h) followed by an fMRI retrieval

Modulation of decision evidence: effect of encoding strength on source memory accuracy

We first examined whether the manipulation of evidence for source memory decisions specifically affected the drift rate of a drift diffusion model applied to the behavioral data of the speeded version of the task. According to the BIC, the best parameterization at the meta-subject level was a model in which the drift rate was allowed to freely vary across conditions while the other parameters remained constant (Inline Supplementary Table 1). Consistently, a one-way ANOVA conducted on the

Discussion

Using an experimental design that involved a parametric variation of decision evidence during source memory judgments, we demonstrated that a restricted set of brain regions, including the lateral parietal cortex around the intraparietal sulcus, exhibits several properties that are consistent with a role in representing a decision variable during source memory judgments. Firstly, these regions showed a robust modulation of the mean signal in response to the manipulation of decision evidence.

Competing interest

We have no financial and non-financial competing interests to declare.

Funding

This study was supported by a grant from University G. d’Annunzio (ex 60%) to C.S.

Acknowledgments

We thank Dina Di Pietro for her assistance on data collection of the pilot experiment.

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