Research report
Human memory manipulated: Dissociating factors contributing to MTL activity, an fMRI study

https://doi.org/10.1016/j.bbr.2011.12.034Get rights and content

Abstract

Memory processes are mainly studied with subjective rating procedures. We used a morphing procedure to objectively manipulate the similarity of target stimuli. While undergoing functional magnetic resonance imaging, nineteen subjects performed a encoding and recognition task on face and scene stimuli, varying the degree of manipulation of previously studied targets at 0%, 20%, 40% or 60%. Analyses were performed with parametric modulations for objective stimulus status (morphing level), subjective memory (confidence rating), and reaction times (RTs). Results showed that medial temporal lobe (MTL) activity can be best explained by a combination of subjective and objective factors. Memory success is associated with activity modulation in the hippocampus both for faces and for scenes. Memory failures correlated with lower hippocampal activity for scenes, but not for faces. Activity changed during retrieval on similar areas activated during encoding. There was a considerable impact of RTs on memory-related areas. Objective perceptual identity correlated with activity in the left MTL, while subjective memory experience correlated with activity in the right MTL for both types of material. Overall, the results indicate that MTL activity is heterogeneous, showing both linear and non-linear activity, depending on the factor analyzed.

Highlights

► Morphed stimuli were used to obtain gradual memory weakening. ► Faces and scenes elicited hippocampal activity during encoding and retrieval. ► MTL activity correlated with a combination of subjective and perceptual factors. ► Reaction times were highly correlated with activity in MTL areas.

Introduction

The medial temporal lobe (MTL) is the main structure involved in long-term memory processes. Considerable effort has been devoted to understand its precise role, as well as the potential for different MTL substructures to be involved in different aspects of memory formation and retrieval. One such dissociation involves spatial and non-spatial materials. For example, Bellgowan et al. ([52]; see also [1]) found higher laterality indices for spatial encoding in the right MTL, and higher laterality indices for object encoding in the left MTL. The face–scene specialization has been proposed to occur in different substructures as well. For example, hippocampus has been proposed to subserve scene processing while perirhinal cortex (PRc) specializes on face processing [2], [3], [4]. This pattern has not been confirmed in other studies, where similar activity for faces and scenes has been observed in perirhinal cortex [1], [5]. More recently, a gradual pattern of activity has been shown for spatial stimuli in the anterior–posterior axis of the parahippocampal gyrus (PHg; [6]).

Another specialization of the MTL areas is proposed to rely on the distinction between recollection and familiarity. Familiarity is described as a quantifiable sensation of knowing the stimulus, while recollection implies a qualitative retrieval of contextual information related to the stimulus (name, color, context, profession, etc.; for a review, see [7]). Neuroimaging studies have shown that recollection is related to hippocampal activation, while familiarity is related to perirhinal cortex activation ([8], [9], [10], [11], [12], [13], [14], [15]; but see [78]). Furthermore, patient studies confirm that hippocampal damage impairs recollection rather than familiarity [4], [16], [17], [18]. Typically, these dual-process investigations rely on meta-memory judgments made by the subject to express the retrieval experience. On the contrary, the discrimination between familiarity and recollection is not adopted by all authors [19], [20], and it has been suggested that, if this dissociation exists, the two processes contribute to a similar degree to the meta-memory judgments made by subjects [21], [22]. In support of this view, recent studies have revealed the tendency of remember–know decisions to be susceptible to experimental instructions [23], [24], evidencing the instability of subjective labeling of memory quality. Furthermore, a meta-analysis of many published studies that used the remember–know procedure showed a single underlying cognitive process for both “remember” and “know” responses [25], [26].

Differently from confidence rating or remember–know responses, source recollection has been claimed to be a “process pure” measure of recollection. However, it has been shown that source retrieval can depend on familiarity in cases when stimulus and context has been unitized into a single representation ([27]; for a review, see [28]).

The exclusive role of the MTL in memory processes has been recently questioned by the “perceptual–mnemonic” hypothesis. According to this hypothesis, MTL plays a role in both perceptual and memory processes, while memory deficits are often mixed with and result from perceptual deficits occurring after MTL damage [29], [30], [31], [32]. This view is supported by single neuron-recordings [33] and non-mnemonic tasks [34], which demonstrate the involvement of MTL activity in both perceptual and mnemonic processes.

A full understanding of cognitive representations in the MTL requires the comprehension of the complex relationship between perceptual status of the stimulus and subjective retrieval experience. However, while memory feelings can be expressed in a graded confidence scale, the perceptual status of the stimulus is categorical: the stimulus is either old or new. Extending this traditional procedure, an objective manipulation of the stimulus may be of high importance for further elucidation of the relationship between variable oldness of stimuli and subjective memory strength. The present study used a gradual morphing procedure to obtain a controlled scale of the status of the stimulus. Two types of stimuli have been investigated in the realm of visual memory, faces and scenes. The manipulation has been carefully calibrated between the two stimuli and neuroimaging data has been analyzed by mean of parametric modulations.

Section snippets

Stimuli

Two sets of stimuli, one for scenes and one for faces were created. Faces contained 96 pairs (48 females) of grayscaled pictures used previously in other experiments [35], [36]. Each pair was newly morphed for this study by placing corresponding dots to the facial features (eyes, eyebrows, hair, etc.; Abrosoft Fantamorph 3 software). The resulting morphed pair produced a gradual change from 0% (Face 1) to 100% (Face 2) in steps of 5% (Fig. 1-A).

Scenes comprised 96 high-resolution pictures of

Behavioral results

Given the actual interest on dual process models, recollection and familiarity estimates were obtained for each morphing step. This procedure takes into account the distribution of responses over the whole experiment to extract a single value of recollection/familiarity for each subject ([44]; algorithm updated to account for random errors; available at http://www.rub.de/neuropsy/tests/memorysolve.zip). Fig. 3 shows familiarity and recollection estimates in relation to morphing steps. Using

Discussion

The aim of the current study was to elucidate the relationship between different factors contributing to MTL activity during recognition memory. A stimulus manipulation procedure was introduced parallel to the classic subjective confidence ratings. In a novel approach, the manipulation procedures were extended to both faces and scenes in a single common function of perceived morphing levels (see Supplemental Material–Appendix A). The first outcome of this procedure was the possibility to

Acknowledgments

This work was funded by a grant (SFB 874) from the German Research Foundation (Deutsche Forschungsgemeinschaft, DFG) to B.Suchan (Project B8). It was also partially funded by the Novobrain Program (Marie Curie Fellowship Association) and supported by the Ruhr-University Research School funded by the German Research Society (DFG) in the framework of the Excellence Initiative. The suggestions of Dr. Julia Weiler have been helpful during the preparation of the manuscript.

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