Establishing associations between pieces of information is related to the medial temporal lobe (MTL). However, it remains unclear how emotions affect memory for associations and, consequently, MTL activity. Thus, this event-related fMRI study attempted to identify neural correlates of the influence of positive and negative emotions on associative memory. Twenty-five participants were instructed to memorize 90 pairs of standardized pictures during a scanned encoding phase. Each pair was composed of a scene and an unrelated object. Trials were neutral, positive, or negative as a function of the emotional valence of the scene. At the behavioral level, participants exhibited better memory retrieval for both emotional conditions relative to neutral trials. Within the right MTL, a functional dissociation was observed, with entorhinal activation elicited by emotional associations, posterior parahippocampal activation elicited by neutral associations, and hippocampal activation elicited by both emotional and neutral associations. In addition, emotional associations induced greater activation than neutral trials in the right amygdala. This fMRI study shows that emotions are associated with the performance improvement of associative memory, by enhancing activity in the right amygdala and the right entorhinal cortex. It also provides evidence for a rostrocaudal specialization within the MTL regarding the emotional valence of associations.
Episodic memory refers to the capacity to recollect individual events [
It is now generally accepted that the medial temporal lobe (MTL) is involved in processing episodic events, but the exact nature of the contribution of its different parts is still a matter of debate. The MTL is composed of the amygdala, the hippocampus, and surrounding cortices (i.e., the perirhinal, the entorhinal, and the parahippocampal cortices). In nonhuman primates, the perirhinal and parahippocampal cortices, and to a lesser extent the entorhinal cortex, receive projections from unimodal and polymodal sensory cortices. In turn, MTL cortices, and mainly the entorhinal cortex, provide inputs to the hippocampus [
Most of studies on associative memory were conducted using neutral materials, limiting their ecological validity, as people encounter multiple emotional stimuli and experience various affective states in their live. To overcome this limitation, emotion must be taken into account [
Most neuroimaging studies that have investigated the effects of emotion on memory were limited to item memory [
In the current study, we used fMRI to investigate the neural correlates of the effects of emotion on associative memory. In light of previous work, we systematically examined MTL activations, as well as the interactions between amygdala activity and both hippocampal and MTL cortical activity.
Twenty-five participants (16 males; 18–29 years) were recruited by means of advertisements placed in local newspapers. All were right-handed as established by the Edinburgh Inventory (
The ethics board of the Montreal Neurological Institute (MNI) approved the study. Each participant signed an informed consent form prior to the experiment and received financial compensation for their participation.
Prior to scanning, participants were provided with a detailed description of the task and instructions. Participants were instructed to memorize pairs of images. They were explicitly asked to memorize both images and also their pairing. Then, a short practice session was administered in order to familiarize participants with the experimental task.
The experimental task was adapted from that initially developed by Touryan et al. [
Illustration of the behavioral task. The left part represents a segment of the encoding session, with pairs composed of a scene and an unrelated common object presented in one of the four corners. The right part represents the pair recognition test during which intact and rearranged pairs were presented.
Approximately 10 minutes after completing the encoding session, participants were required to make a pair recognition judgment. No functional scanning was conducted during the associative recognition test. Participants were presented with 90 consecutive trials (45 intact pairs and 45 rearranged pairs) and were instructed to indicate whether pairs were intact (objects and scenes presented in the same pairing as in the encoding session) or rearranged (pictures previously studied but presented in a new pairing). For rearranged pairs, the object was located in the same corner as during encoding to control for potential source memory effects. Additionally, a given object, if presented at encoding with a negative scene, was rearranged with another negative scene at recognition and not with a positive or neutral scene. The use of rearranged pairs as lures is designed to avoid judgment based on the familiarity of items. Thus, accurately rejecting rearranged pairs requires explicit knowledge of stimuli as well as their association.
Approximately 30 minutes after completing the recognition session, a cued recall test and a valence rating task were administrated outside the scanner. We included a cued recall test to determine how an emotional stimulus (i.e., the scene) influences the between-stimuli binding of a neutral stimulus (i.e., the object). We also included a valence rating task since we were interested in confirming that the participants considered the emotional pictures as emotional and the neutral pictures as neutral. In both the cued recall test and the valence rating task, the central scenes were presented again but without any objects. In the cued recall test, participants were asked to (i) recall from memory the object that was presented with the scene during encoding; and (ii) indicate in which corner it was presented, even if they could not recall the objects themselves. During the valence rating task, participants were asked to rate the emotional valence of each visual scene using a 9-point Likert scale ranging from 1 (extremely negative) to 9 (extremely positive), with 5 indicating a neutral valence. The order of these two tasks was fixed, with the cued-recall test first and the valence task second.
Scanning was carried out on a whole-body 1.5T Siemens Sonata System, using gradient-echo EPI sequences. The head was stabilized with a moldable vacuum cushion to minimize head movements. First a localizer scan was acquired followed by the functional run consisting of 214
Behavioral performance was analyzed using Statistica 6.0 (Statsoft). In order to estimate pair recognition accuracy separately from response bias, a primary recognition index was examined using the Two-High Threshold Theory [
In all behavioral analyses, the alpha level was set at 0.05.
Functional images acquired during memory encoding were pretreated with SPM5 (
To assess the effects of emotion on associative memory, four event types were modeled: positive, negative, and neutral associations and the fixation cross (baseline). Positive and negative trials were pooled into a single condition named “emotional” condition, as analyses revealed no significant differences between positive and negative valence conditions for either behavioral performance (
Data are summarized in Table
Mean (and SEM) proportions of hits (H), false alarms (FA), Pr index, and recall score as a function of emotional associations and neutral associations conditions.
Recognition | Recall | |||
---|---|---|---|---|
H | FA | Pr | ||
Emotional associations | 0.80 (0.03) | 0.15 (0.04) | 0.63 (0.04) | 0.33 (0.04) |
Neutral associations | 0.79 (0.04) | 0.20 (0.03) |
|
|
Two participants were excluded from fMRI analyses as they failed to reach criterion for performance during the encoding phase (<75% correct responses for the object-location judgment). The 23 remaining participants achieved above 96% correct responses (mean: 99%; SEM: 0.22), a performance level clearly indicative of full attention during stimulus presentation.
Whole brain analyses revealed that emotional associations activated predominately posterior regions, relative to neutral associations. Activations were observed in occipital (inferior and middle gyri), cuneus, parietal (postcentral, supramarginal gyri, and precuneus), temporal (middle, superior and fusiform gyri, entorhinal cortex), frontal (precentral superior frontal gyri, cingulate), and subcortical (substantia nigra and reticular formation) areas. Conversely, neutral associations elicited greater activations than emotional associations, predominately in anterior regions, including the cingulate (posterior and anterior gyri), temporal (superior and parahippocampal gyri), and frontal (middle and inferior gyri) areas. The conjunction analysis revealed that both emotional and neutral associations induced activations in the left premotor cortex and in the left anterior cingulate cortex, as well as in the right caudate nucleus, fusiform gyrus, culmen, and the hippocampus. Details about all these activations are reported in Table
Activations elicited by encoding when contrasting the emotional and neutral conditions.
Cerebral domain | BA |
|
Stereotaxic coordinates | Cluster size (voxels) | ||
---|---|---|---|---|---|---|
|
|
| ||||
Emotional > neutral | ||||||
Middle occipital gyrus (R) | 19 | 4.54 | 48 | −76 | 0 | 231 |
Postcentral gyrus (L) | 3 | 4.51 | −52 | −26 | 58 | 73 |
Cuneus (R) | 18/19 | 4.30 | 12 | −88 | 14 | 150 |
Inferior occipital gyrus (L) | 18 | 3.96 | −38 | −86 | −18 | 25 |
Fusiform gyrus (R) | 37 | 3.94 | 36 | −52 | −22 | 66 |
Posterior cingulate gyrus (L) | 31 | 3.86 | −14 | −42 | 42 | 42 |
Inferior occipital gyrus (R) | 17 | 3.85 | 28 | −96 | −6 | 43 |
Middle temporal gyrus (L) | 19 | 3.81 | −52 | −72 | 14 | 75 |
Culmen | 3.76 | 16 | −66 | −12 | 26 | |
Superior frontal gyrus (R) | 8 | 3.71 | 24 | 40 | 52 | 35 |
Entorhinal cortex (R) | 28 | 3.65 | 26 | −12 | −32 | 15 |
Precuneus (L) | 19 | 3.63 | −2 | −78 | 38 | 53 |
Inferior occipital gyrus (L) | 18 | 3.62 | −28 | −98 | −10 | 24 |
Posterior cingulate gyrus (R) | 30 | 3.56 | 4 | −48 | 18 | 84 |
Supramarginal gyrus (L) | 40 | 3.55 | −50 | −46 | 32 | 19 |
Substantia nigra | 3.55 | 12 | −12 | −8 | 12 | |
Superior temporal gyrus (R) | 22 | 3.50 | 54 | −60 | 14 | 16 |
Pons (reticular formation) | 3.49 | −2 | −28 | −36 | 13 | |
Precentral gyrus (L) | 6 | 3.47 | −52 | 6 | 38 | 27 |
Precuneus (R) | 7 | 3.46 | 12 | −58 | 30 | 41 |
Fusiform gyrus (R) | 19 | 3.37 | 32 | −78 | −12 | 12 |
Pulvinar | 3.32 | −10 | −30 | 12 | 13 | |
|
||||||
Neutral > emotional | ||||||
Parahippocampal gyrus (R) | 36 | 4.28 | 16 | −36 | −16 | 24 |
Middle frontal gyrus (R) | 46 | 4.19 | 32 | 44 | 16 | 17 |
Superior temporal gyrus (R) | 22 | 3.96 | 50 | −6 | −4 | 22 |
Inferior frontal gyrus (L) | 46 | 3.73 | −34 | 34 | 12 | 21 |
Parahippocampal gyrus (R) | 36 | 3.63 | 24 | −42 | −6 | 12 |
Posterior cingulate gyrus (R) | 23 | 3.48 | 22 | −32 | 28 | 13 |
Anterior cingulate gyrus (R) | 33 | 3.41 | 10 | 12 | 22 | 15 |
|
||||||
Emotional | ||||||
Caudate nucleus (R) | 4.26 | 22 | 20 | 18 | 65 | |
Fusiform gyrus (R) | 37 | 3.86 | 34 | −56 | −10 | 168 |
Anterior cingulate gyrus (L) | 24 | 3.44 | −20 | −2 | 34 | 33 |
Precentral gyrus (L) | 6 | 3.44 | −48 | −8 | 22 | 41 |
Precentral gyrus (L) | 4 | 3.05 | −22 | −18 | 50 | 10 |
Culmen | 2.85 | 30 | −40 | −28 | 12 | |
Hippocampus (R) | 36 | 2.62 | 32 | −28 | −12 | 10 |
L: left, R: right, and BA: Brodmann area.
Restricted analyses focusing on the MTL showed that emotional associations induced greater activations in the right entorhinal cortex (26/−12/−32;
Illustration of activations revealed by ROI analyses. Emotional associations induced greater activations than neutral associations in (a) the right amygdala (
The mean activation level in each of these four clusters was then evaluated. Using the amygdala modulatory hypothesis as a model to explore MTL interregional covariation in activity [
This event-related fMRI study yielded three main results. First, participants had better memory performance for emotional than for neutral associations. This enhancement was observed for both recognition and recall test modalities. Second, rostrocaudal dissociation within the medial temporal lobe was observed as a function of the emotional valence of associations: greater activations were found in the entorhinal cortex for emotional associations while greater activations were found in the posterior parahippocampal gyrus for neutral associations. In addition, amygdala activity had an opposite effect on entorhinal and parahippocampal activity. Third, emotional and neutral associations shared common cerebral areas, comprising the hippocampus and other regions belonging to an attentional network.
As previously mentioned, the behavioral effects of emotion on associative memory are mixed [
In our study, participants were more accurate in recognizing emotional associations than neutral associations. Similarly, participants better recalled objects and their location when these were associated with emotional scenes than neutral scenes. These results converge with many previous findings [
Within the right MTL, we observed a functional specialization along the longitudinal axis: encoding emotional associations led to enhanced activations in the entorhinal cortex, whereas encoding neutral associations led to enhanced activations in the posterior parahippocampal cortex. Such rostrocaudal dissociation has already been demonstrated with IAPS pictures [
Previous hypotheses with respect to rostrocaudal dissociation of medial temporal function have been proposed. For instance, a meta-analysis of experimentally induced changes in blood flow (“activation”) in positron emission tomography (PET) studies of memory revealed such functionally dissociation between rostral and caudal regions of the hippocampal formation [
In parallel with the functional specialization of MTL cortices, the conjunction analysis revealed that the right hippocampus was activated by both emotional and neutral associations, regardless of amygdala activity. This result is consistent with the proposal that the hippocampus binds distinct elements of an event into an integrated representation [
In addition to the hippocampal activation, greater activations were also induced by both emotional and neutral associations in various areas subserving attentional processing. For instance, common activations were found in the premotor cortex, the posterior part of the fusiform gyrus, and the dorsal part of the anterior cingulate gyrus. This pattern of activations has been consistently found in tasks demanding spatial attention [
One limitation of this study is that interactions between amygdala activity and hippocampal and MTL cortices activity rely on correlation analyses, which do not indicate the direction of these interactions. Further analyses examining effective connectivity should be performed to overcome this limitation. Another limitation of this study is the lack of a condition assessing the processing of individual stimuli. At the current level, it remains difficult to straightforwardly conclude that the results were driven by associative processes per se, rather than by emotions. Lastly, the subsequent memory effect, which represents the difference during encoding between brain activity for items that are subsequently remembered and brain activity for items that are subsequently forgotten [
With respect to previously published data, our results confirm that the hippocampus, in concert with attentional network regions, participates in the encoding of associations in memory. Our results also extend past findings by demonstrating that emotions are associated with the performance improvement of associative memory. This potentiation may result from enhanced activity in the right entorhinal cortex by the right amygdala. Future research may consider functional connections among these cerebral structures to elucidate the neural mechanisms assuming their respective functions.
The authors declare that there is no conflict of interests regarding the publication of this paper.
This study was supported by an operating grant from NSERC. Drs. Lepage Martin and Luck David are supported by a salary award from the