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. Author manuscript; available in PMC: 2013 Mar 12.
Published in final edited form as: Top Magn Reson Imaging. 2009 Oct;20(5):271–278. doi: 10.1097/RMR.0b013e3181e8f1f9

fMRI Evidence For Binding And Consolidation Pathways For Face Name Associations: Implications For Associative Memory Disorder

Melissa Robinson-Long 1, Jianli Wang 2, Qing X Yang 2, Mark Meadowcroft 2, Xavier Golay 5, Paul J Eslinger 1,2,3,4
PMCID: PMC3595016  NIHMSID: NIHMS276788  PMID: 20859188

Abstract

Objective

To determine common and distinctive brain activation patterns associated with encoding and recognition of face-name associations and identify the neural structures with BOLD amplitude differences specific to binding and memory consolidation processes.

Methods

Five healthy adult participants viewed face-name pairs during the encoding phase and completed the multiple choice recognition memory task after a brief delay. BOLD response amplitudes in specific regions of interest and whole brain activation maps were analyzed.

Results

Common activations were observed in encoding and recognition memory tasks in several ROI encompassing the medial temporal and occipital regions. Higher amplitudes occurred in right fusiform gyrus and right hippocampus during encoding. In contrast, higher BOLD response amplitudes were detected in the lingual gyrus bilaterally during recognition memory. Encoding activated distributed prefrontal and temporal cortical regions bilaterally that spanned attentional, executive, language, and memory systems. Recognition memory recruited convergence zones in the left prefrontal cortex and the parietal-occipital-temporal region bilaterally where multimodal visual association, language, memory and decision-making systems interact.

Conclusions

The higher right fusiform gyrus and right hippocampus activation during encoding suggests a potentially specific binding pathway. The increased lingual gyrus BOLD response during recognition memory may indicate a neural substrate for memory consolidation and long-term knowledge. Average activation maps revealed task-specific differences in areas of the prefrontal, temporal, and occipital-parietal-temporal cortices. Findings suggest that lesions in fairly widespread cerebral regions may potentially disrupt specific binding or memory consolidation processes.

Keywords: fMRI, encoding, memory retrieval, face name processing

Introduction

Since reliable fMRI methods have been established, brain activations associated with memory and cognitive processes have been investigated in order to identify both the anatomical and physiological substrate for these complex adaptive behaviors. Contemporary fMRI research is focused in part on undertaking a more in depth investigation of brain-behavior relationships than may be possible with clinical lesion studies. This can include contrasts according to age, gender, and multiple task parameters as well as localized anatomical and networking analyses (Miezin et al., 2000). In this study, we utilized fMRI to investigate brain activation patterns and BOLD response differences of anatomical regions specific to associative learning and memory of an essential set of stimuli for everyday functioning, namely face- name pairs. Such memory complaints are common in clinical conditions of traumatic brain injury, Alzheimer's disease, and major depression. Face- name learning and memory are also important areas of research for understanding social cognition (Haxby et al., 2000), aging-associated cognitive changes, and face-specific processing disorders such as prospoagnosia (Marotta et al., 2001). However, the neural substrate for face-name learning is minimally understood.

In extant literature, several studies have focused on brain activations related to viewing faces only (Allison et al., 1994, Clarke et al., 1997), face processing vs. non-face objects (Haxby et al., 1991, Chao et al., 1999, Duchaine and Nakayama, 2005), faces associated with emotions (Sprengelmeyer et al., 1998, Blair et al., 1999, Kilts et al., 2003), scrambled or inverted faces (Clark et al., 1998, Collishaw and Hole, 2000), and brain activations during viewing of famous and/or familiar faces (Leube et al., 2003; Leveroni et al., 2000, Bernard et al., 2004). A smaller set of studies have investigated learning of face-name pairs with widely different cognitive, electrophysiological and brain imaging methods (Joassin et al., 2004; Kirwan & Stark, 2004, Naveh-Benjamin et al., 2004, Gimenez et al., 2005; Groninger, 2006; Tsukiura et al., 2006), but none have specifically analyzed functional brain activations and BOLD response amplitudes during both encoding and recognition of face-name pairs across multiple anatomical areas (i.e., medial temporal lobe and visual cortex. Although much research has contributed to the study of the brain's response to faces and to face-name pairing, there is still considerable ambiguity related to the neural substrate for such learning and memory. To our knowledge, there have been no region of interest (ROI) studies focused on specific neural structures in the medial temporal lobe and occipital lobe thought to mediate encoding and consolidation of face-name pairs, not fMRI studies to evaluate the BOLD response peak amplitude parameter, allowing comparison of ROI's and their level of involvement in each task. We were thus interested in analyzing face and name pairing involved in an encoding as well as retrieval task by using fMRI and comparing structures level of involvement in each task.

Based upon the clinical and basic neuroscience literatures regarding anatomical regions involved in learning and memory, we chose eight regions of interest that we suspected would be involved in the associative face-name encoding and retrieval tasks. These regions span visual association cortex, medial temporal lobe, and the prefrontal cortex, and include: 1) anterior fusiform, 2) posterior fusiform, 3) hippocampus, 4) lingual gyrus, 5) occiptital middle gyrus, 6) temporal inferior gyrus, 7) occipital inferior gyrus, and the 8) dorsolateral prefrontal cortex (PFC). Within each ROI, we were interested in analyzing the BOLD response peak amplitude and comparing the response differences between tasks as well as between ROI structures. Such knowledge may be important for understanding the structures involved in associative learning and memory as well as the similarity and distinctiveness of their roles in each task.

Based on previous findings (Andreasen et al., 1996, Eslinger et al., 1996, Verstichel, 2001, Henson et al., 2003, Kirwan and Stark, 2004) we predicted that of the eight ROI's that we chose, the structures of greatest interest in these tasks would be the posterior fusiform, the prefrontal cortex, and the hippocampus. The posterior fusiform gyrus, particularly on the right side (Kim, Andreasen et al. 1999, (Hoffman and Haxby, 2000, Takahashi and Kawamura, 2002) is very popular in the study of the brain's response to human faces. It is widely known as the “face area” of the brain. The hallmark symptom of unfortunate disease, known as prospoaganosia, is the inability to recognize faces and occurs due to damage to this face processing area (Bodamer, 1947). Because of the fusiform gyrus' evident role in face processing, one would suspect that the BOLD response to faces in this region would then be similar for both the tasks considering both tasks involve faces. Previous findings support that this structure is indeed involved in both tasks, but at different levels (Zeineh et al., 2003). Thus, we expected to find a higher BOLD response peak amplitude in the encoding task because of the novelty of the faces and the perceptual component involved and less activation in retrieval due to familiarity and other processes taking place in other structures (Rhodes and McLean, 1990, George et al., 1999). Recent studies also indicate this structure to be activated as an “expertise” effect or processing due to encoding of a unique individual (Gauthier et al., 2000). From this information, we predicted that there would be a significant BOLD response in the posterior fusiform (higher on the right side) in the encoding task vs. the retrieval task.

The hippocampus was the second major region of interest of study. Despite,the popular thought that the hippocampus is tied to memory recognition, recent studies (Clarke et al., 1997, Eichenbaum, 1997, Guo et al., 2005) show that it is more involved in making memories and associations, or as Cohen, Ryan et al. (Cohen et al., 1999) describes the hippocampus as a mediator of “memory binding.” In this study, participants were required to associate or “bind” a face with a name. We predicted that the hippocampus would be more highly involved in the encoding task and to a higher extent on the right side, as suggested by Kirwan and Stark (2004).

Lastly, we sought to analyze was the dorsolateral PFC. Many studies suggest that the PFC is highly involved in memory retrieval (Buckner et al., 1999, McDermott et al., 1999, Rugg et al., 1999, Konishi et al., 2000), particularly on the left side (Cansino et al., 2002). While the left PFC appears to be biased toward language processing (Puce et al., 1996, Cohen et al., 2000), it has also been implicated in the encoding of faces and names (Haxby et al., 1994, Summerfield et al., 2006). Combining these findings, we predicted that the left PFC would be have a higher BOLD response during encoding because of the name/word component as well as the highly associative demands of face-name pairing.

Materials and Methods

Study Participants

The fMRI protocol was conducted on 5 healthy, volunteer participants 20-50 years of age (4 male, 1 female). All subjects had at least a high school education.

fMRI Study Procedures

Preparation and Positioning

The present study was carried out on a 3.0 tesla Philips MRI scanner (Philips Medical Systems, the Netherlands). Subjects laid flat in a head restrainer which minimized the amount of motion as well as provided proper positioning and comfort. We used a boxcar paradigm, consisting of alternating intervals of baseline and cognitive activation. During scanning, subjects responded to visual stimulation by pressing the buttons on a fiber optic button box.

Image Acquisition

Data was acquired by the MRI scanner. A T1 –weighted three-dimensional image (3-D TFE) was acquired for anatomical structure with time of repetition (TR)/ echo time (TE)/ flip angle (FA)=8.05ms/ 3.7ms/ 8°, FOV=256 × 150 mm3, acquisition matrix=256 × 256×150, and a SENSE factor =2. Echo planar imaging (EPI) was used for data acquisition with TR=3600ms, TE=30ms, FA=90°, 28 axial slices, slick thickness=2.5 mm, FOV=210 × 210 mm3, acquisition matrix=80 × 80, reconstruction resolution=128 × 128, and SENSE factor=2 . Two tasks were administered in each imaging session. For each session, 64 images were acquired during 8 blocks of stimulation and baseline. Each subject underwent two runs.

Encoding and Memory Recognition Paradigms

Black-and-white faces with hair removed and names displayed below were viewed through a reflection mirror in front of the eyes of the subject. Images were presented using E-Prime software (Psychology Software Tools, Inc, Pittsburg, PA, USA). The first task was an encoding task where the subjects viewed 16 faces paired to an uncommon first name (8 males, 8 females). Each face-name pair was presented for 3.6s. After 4 face-name pairs were presented, the baseline, which was a screen with a plus, would be displayed for 14.4s. During the second task, which alternated with each 4 face-name encoding block, the subjects would view a face with a choice of four names. The subjects were required to recognize the face-name pair and press the corresponding button (one of four) on the control device. Each face and choice of four names was presented for 3.6 seconds. There were a total of 16 face (each with four names) stimuli, divided into 4 blocks. After each recognition block, there was a 14.4 s baseline. The total scan duration was 230.7s.

Data Analysis

The fMRI data collected during the tasks was processed with SPM2 software (Wellcome Department of Cognitive Neurology, London, UK) implemented in Matlab (Mathworks, Inc.). Functional images were re-aligned to remove any minor movements. The anatomical high resolution T1-weighted images were co-registered with fMRI images and spatially normalized to the Montreal Neurological Institute brain template. The time-course images were normalized using the same normalization parameters and then smoothed with a 6×6×8 mm3 Gaussian smoothing kernel. A statistic parametric map (SPM) was generated for encoding and retrieval tasks by fitting the stimulation paradigm to the functional data which was convolved with a hemodynamic response function. Activation from the baseline paradigm was subtracted from the stimulation paradigms, allowing us to see activation specific to encoding and retrieval processes. For group analysis, average activation maps were generated (one-sample t- test, p<.001). Group activation maps that subtracted the opposite task activation were generated by a paired t-test (p<.001). For BOLD response amplitude measurements (units measured in signal change percentage), each subject's time course was averaged to give a hemodynamic curve from which the height could be recorded. T-tests (two-sided) were used to compare encoding and retrieving stimulation within several regions of interests.

Results

Subjects performed with an average accuracy of 41.41% (SD±12.02%) in the retrieval of face-name pairs. The average response time for the tasks was 1828.91ms (SD±390.07ms).

Activation maps for the encoding and memory recognition tasks were analyzed with summary of activated clusters in Table 1. Across the 2 tasks, there were common, prominent activations detected in primary visual cortex and multiple secondary visual areas including extensive portions of Brodmann's areas 18 and 19 bilaterally (mainly in the inferior infracalcarine regions) but with notable extension to occipital-temporal regions (areas 37 and 20/21) as well as occipital-parietal and cuneus regions. There were also common hippocampal activations bilaterallyfor the 2 tasks. When encoding and memory recognition conditions were contrasted, more specific distinctions were observed (see Figure 1). Results indicated that during encoding , hippocampal regions were activated bilaterally, whereas during memory recognition, the most prominent activations occurred in the visual association areas.

Table 1.

Summary of Significant Activations Identified during Associative Encoding and Memory Recognition Tasks

Brodmann area Talairich coordinates voxels (k)
Anatomical Region BA x y z Encoding Retrieval
Calcarine R 17/18 12 -88 8 498 492
Fusiform L 19/37 -42 -42 -20 353 182
Fusiform R 19/37 41 -43 -20 325 311
Occipital Mid L 18/19 -32 -80 5 306 196
Occiptal Mid R 18/19 37 -80 -1 277 241
Occipital Inf R 17/18 38 -88 -5 260 116
Occipital Inf L 17/18 -32 -88 -6 251 163
Temporal Inf L 20/21 -53 -57 -12 250 154
Lingual R 18 19 -63 -11 240 404
Calcarine L 17/18 -6 -88 -6 207 296
Lingual L 18 -16 -56 -7 190 299
Temporal Inf R 20/21 50 -52 -18 188 74
Occipital Sup R 19 28 -71 40 165 127
Cuneus R 18/19 11 -87 20 109 158
Occipital Sup L 19 -20 -84 23 107 127
Cuneus L 18/19 -9 -86 24 88 129
Anterior fusi R 20 30 -6 -35 23 17
Anterior fusi L 20 -30 -4 -35 10 13
Hippocampus L 28/35 -31 -18 -16 15 10
Hippocampus R 28/35 22 -13 -16 18 21
PFC R 47 -42 34 25 14 18
PFC L 47 -50 20 21 12 14
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Note: For the regions included under the encoding and retrieval regions heading, a one-sample t-test was used and an uncorrected p<.001. For the structures under the encoding regions only and retrieval regions only headings, a paired t-test was used and an uncorrected p<0.001.

Figure 1.

Figure 1

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Activation clusters associated with encoding and memory recognition tasks. Red represents activations specific to encoding in contrast to memory recognition. Blue represents activations specific to memory recognition in contrast to encoding. (Level of axial slice noted by z coordinate). P =.005 with a 10 voxel threshold.

Location of the eight specific ROI are shown in Figure 2. We measured the BOLD response amplitude response for each task in each ROI and then compared the amplitude difference between encoding and memory recognition tasks in each structure. The results are shown in Figure 3. Specifically, in the encoding task, both the right posterior fusiform [E (encoding) A (amplitude) = 0.226, R (recognition) A (amplitude) = 0.112; p=0.027], and the right hippocampus (EA = 0.182, RA = 0.011, p.= 0.013) generated significantly higher BOLD response amplitudes than in the memory recognition task. The right anterior fusiform (EA = 0.225, RA = 0.130, p = 0.073) approached significance in respect to higher BOLD response amplitude during encoding vs. memory recognition. In the memory recognition task, the right lingual gyrus BOLD response (RA = 0.331, EA = 0.215, p = 0.07) also approached significance while the left lingual gyrus (RA =.304, EA = .095, p = 0.003) was significantly higher in comparison to the encoding task. We did not detect significant differences in BOLD response between encoding and recognition tasks in the remaining ROIs.

Figure 2.

Figure 2

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The eight regions of interest chosen for comparison of the BOLD response between encoding and memory recognition tasks.

Figure 3.

Figure 3

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Structures that had a significant or an approaching significance difference in BOLD response between encoding and retrieval tasks. P<.001 used for posterior fusiform right (post fusi r), and lingual gyrus right and left (ling r and l). P<.001 used for anterior fusiform right (anti fusi r), and hippocampus right (hippo r).

With regard to large scale cerebral activation patterns for encoding and memory recognition, we were interested in identifying general trends in activation differences between the tasks. During encoding, there were much broader right frontal-temporal activations, whereas memory recognition recruited a broad expanse of posterior temporal-occipital-parietal cortices bilaterally and left prefrontal activity (see Figure 4 for 3-D representations).

Figure 4.

Figure 4

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Average activation maps overlaid on a 3D- image of the brain. Red represents encoding activations. Green represents memory recognition activation. (p=.005 with a threshold of 10 voxels).

Discussion

Findings support the conclusion that there are clear and consistent brain activation differences related to associative encoding and memory recognition processes, suggesting somewhat distinct neural substrates. Associative encoding of face-name information aligned with significantly increased BOLD response amplitudes in the right posterior fusiform gyrus and right hippocampus in healthy adults. In contrast, BOLD response amplitudes were increased in the lingual gyrus during subsequent memory recognition. These findings suggest that the right hippocampus may be more involved in the information binding or associative mechanisms of face-name encoding, consistent with the observations of Kirwan and Stark (2004) as well as Cohen (1999), but also add an important extension to the neural substrate. That is, increased BOLD response amplitude was concurrently detected in the right posterior fusiform gyrus, a known face-processing area, suggesting that encoding may also depend upon linkages of the hippocampus with cortical processing areas. The right anterior fusiform region showed a trend toward a difference between tasks with a higher BOLD response during encoding, though we are uncertain whether this was due to its proximity to the hippocampal region and the networking of the neural structures involved in encoding.

Contrast of memory recognition to encoding identified a unique increase in the BOLD response amplitude in the lingual gyrus, which as a visual association area may be critical to long-term representation of acquired knowledge. Contrary to our predictions, the BOLD response amplitudes in the PFC were not significantly different between tasks or hemispheres, although the PFC had the highest overall BOLD response amplitude in both tasks compared to the other regions of interests, suggesting an important physiological role in associative processing.

We know that visual information at the cortical level is first processed through the primary visual cortex and then depending on its characteristics may engage either the dorsal/”where” and/or ventral “what” specialized streams. In this case of face-name stimuli, feed-forward pathways from inferior occipital cortex extend to more rostral occipital, temporal and parietal structures (Eacott and Gaffan, 1992; Shen et al., 1999; Haxby et al., 1999, Ishai et al., 1999). Our results support the role of these feed-forward pathways in face-name associative learning and recognition and suggest that pathophysiology from a variety of causes in these regions (e.g., stroke, anoxia, trauma, neoplasm) may have clinically significant disruptive effects on such learning and memory.

With regard to the neural substrate mediating associative face-name encoding, we propose that the right anterior and posterior fusiform regions together with the right hippocampus are key neural resources. Because of the attentional, associative and working memory demands of the task, the PFC is also likely to play a key role during learning (Kanwisher et al., 1997). The PFC is linked closely with the hippocampal region through strong interconnections (Grady et al., 1995, Sperling et al., 2003, Bernard et al., 2004) and likely contributes to how disparate information can be bound in sufficient fashion to be available for consolidation and long-term storage in association cortices (Squire et al., 1992).

Derived from our activation maps, we also found that structures specific for encoding included the superior and middle temporal gyri and the posterior cingulate gyrus in the left hemisphere. The middle temporal gyrus has been implicated in processing names in relation to faces (e.g. (Gorno-Tempini et al., 1998) and the superior temporal gyrus has been linked to social perception of facial characteristics, such as eye gaze and lip movement (Puce et al., 1998). The posterior cingulate gyrus has significance in that it seems to be a connecting pathway between anterior structures and the hippocampus (Goldman-Rakic et al., 1984).

With regard to the neural substrate related to recognition memory for face-name processing, although face stimuli must be processed by the “face structures” such as the fusiform, there is significantly less of a BOLD response than in the encoding task, suggesting that retrieval uses a different network. We detected significantly less activation in the right hippocampus as well, suggesting again that this may not as essential a part of the recognition network for face-name pairs. Our results, however, showed a significantly higher BOLD response amplitude in the bilateral lingual gyrus during recognition, indicating that this structure may mediate more of an important role than previously thought. In recognition, increased activity of the PFC may signal the initiation of a top-down cascade of regulatory processing that works to retrieve episodic visual associations such as face-name pairs from long-term memory (Haxby et al., 1996, Tomita et al., 1999, Joassin et al., 2004, Ranganath et al., 2004).

Recognition memory studies concerning face-name information have not been given as much attention as encoding studies, and therefore do not have overwhelming evidence supporting a specified network, although the medial frontal gyri, the inferior parietal lobe, supramarginal gyrus, and inferior frontal gyrus in the left hemisphere have been raised as possibilities (Gorno-Tempini et al., 1998, Campanella et al., 2001, Leube et al., 2003). We propose that the parietal lobe activations detected from the average activation maps may be of interest. These regions seem to act as convergence zones that are accessible to many cortical association areas including the PFC, and that can provide multimodal resources important for recognition and episodic retrieval (Yonelinas et al. 2005, Culham and Kanwisher 2001, Vincent 2007, Wagner et al. 2005). Taken together, the findings suggest that there are both key regions of processing in the hippocampal and visual association cortices that are necessary for associative encoding and recognition memory of face-name information, as well as processing resources provided by regions of the PFC, temporal and parietal cortices that are vital to effective learning and memory retention. With such a large-scale network, pathophysiology in the form of trauma, cerebrovascular disease, neurodegeneration, and neoplasm can cause symptoms that range from being clinically disabling (from damage to key structures) to milder deficits (from damage to resources areas) that can be managed with compensatory learning and memory strategies.

Abbreviations

fMRI

functional MRI

r

right

l

left

post fusi

posterior fusiform gyrus

ant fusi

anterior fusiform gyrus

hippo

hippocampus

temp inf

temporal inferior gyrus

lingual

lingual gyrus

occ inf

occipital inferior gyrus

occ midd

occipital middle gyrus

PFC

dorsal lateral prefrontal cortex

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