Cortical Representations of Personally Familiar Objects and Places: Functional Organization of the Human Posterior

Motoaki Sugiura1,2,3, Nadim J. Shah1, Karl Zilles1,2, 1,4

and Gereon R. Fink Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/17/2/183/1757137/0898929053124956.pdf by guest on 18 May 2021

Abstract & The recognition of both personally familiar objects and temporal junctions and intraparietal sulci bilaterally. A places involves nonspatial memory retrieval processes, but significant main effect of familiarity with greater activation only personally familiar places are represented as space. in the familiar (FP and FO) than unfamiliar (UP and UO) Although the posterior cingulate cortex (PCC) is considered trials was observed in the mid-dorsal PCC (mPCC), retro- to process both types of such memories, its functional splenial cortex, posterior , and the left intraparietal organization is poorly understood. In this event-related fMRI . Activation specific to the FP trials (as assessed by the study, normal subjects judged familiar/unfamiliar pictures in interaction) was observed in the right posterodorsal PCC four categories: familiar places (FP), familiar objects (FO), (pPCC) only. Together with data from previous functional unfamiliar places (UP), and unfamiliar objects (UO), thus imaging studies, the results suggest a functional segregation constituting a two-factorial design. A significant main effect of of human PCC with differential involvement of pPCC in stimuli with greater activation in the place (FP and UP) than spatial representations of personally familiar places and of object (FO and UO) trials was observed bilaterally in several the mPCC and in episodic retrieval of medial temporo-occipito-parietal regions, including the caudal personally familiar places and objects. Activation of the left PCC (cPCC) and parahippocampal . The reverse compar- intraparietal sulcus may reflect retrieval of memories related ison revealed greater activation in the lateral inferior occipito- to object manipulation. &

INTRODUCTION Recognition of personally familiar objects and places The recognition of familiar objects and places is essential may share neural mechanisms with episodic memory for understanding one’s own situation and for planning retrieval. An object or place becomes ‘‘personally famil- one’s behavior. Visual recognition of a familiar place is iar’’ only through an experience of being there or usually helped by salient objects (i.e., landmarks) and handling it, respectively, and there is no doubt that the accompanying recognition processes of particular many familiar objects and places play an important role objects belonging to the scene. Therefore, visual recog- in specific autobiographical episodes. To our knowl- nition of a personally familiar place is likely to involve edge, failure to recognize personally familiar objects processing of both personally familiar objects and per- despite normal recognition of their general identity sonally familiar space. Our knowledge of brain mecha- has never been reported in patients with brain damage, nisms that support representation of personally familiar except subsidially to the general impairment in retrieval objects and spaces in long-term memory is to date of past episodes (De Renzi, Lucchelli, Muggia, & Spinn- scarce. A previous functional imaging study compared ler, 1995; Markowitsch et al., 1993). On the other hand, activation during presentation of personally familiar it was suggested that patients with lesions of the medial faces and voices with unfamiliar ones (Shah et al., aspect of the occipital or may show 2001). Although a face can be regarded as a class of impairment in recognizing salient environmental fea- objects, it is not evident whether the findings on per- tures with relatively intact ability to recognize familiar sonally familiar people can be extended to familiar objects (landmark agnosia) (McCarthy, Evans, & objects in general. Hodges, 1996; Habib & Sirigu, 1987; Landis, Cummings, Benson, & Palmer, 1986; He´caen, Tzortzis, & Rondot, 1980). These neuropsychological data support the no- 1Forschungszentrum Ju¨lich, Germany, 2Heinrich-Heine-Univer- tion that recognition of a personally familiar place may at sita¨t Du¨sseldorf, Germany, 3Tohoku University, Sendai, Japan, least in part rely on different neural mechanisms than 4Universita¨tsklinikum der RWTH Aachen, Germany those for recognizing personally familiar objects. In the

D 2005 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 17:2, pp. 183–198 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929053124956 by guest on 27 September 2021 light of recent neuropsychological (Epstein, De Yoe, imaging studies (e.g., Henson, Rugg, Shallice, Josephs, Press, Rosen, & Kanwisher, 2001) and functional imaging & Dolan, 1999; Wiggs, Weisberg, & Martin, 1999; studies (Epstein, Harris, Stanley, & Kanwisher, 1999; Buckner, Raichle, Miezin, & Petersen, 1996; Tulving, Epstein & Kanwisher, 1998), the impairment can be Markowitsch, Craik, Habib, & Houle, 1996). In particu- attributed to deficits in visual processing and encoding lar, activation in the PCC during presentation of per- of the large-scale environment supported by the para- sonally familiar faces and voices compared with that of hippocampal gyrus. unfamiliar ones (Shah et al., 2001) is relevant to this Several lines of evidence suggest an important role study. Although the PCC is thus clearly a region of for the posterior cingulate cortex (PCC) in the repre- interest in this study, there exists a serious controversy sentation of personally familiar space and episodic concerning its roles in spatial and nonspatial memory Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/17/2/183/1757137/0898929053124956.pdf by guest on 18 May 2021 memory retrieval. Some patients with lesions in the PCC retrieval (see also Maguire, 2001; Vogt, Absher, & Bush, can recognize a place, but have no sense of direc- 2000; Maddock, 1999; Vogt, Finch, & Olson, 1992). Com- tion there, without deficits in visuospatial integration parison of neural activity between the spatial and non- (Takahashi, Kawamura, Shirota, Kasahata, & Hirayama, spatial memory tasks, which we intend in this study, 1997; Cammalleri et al., 1996). Their deficits may be is particularly relevant to the current controversy re- explained by a breakdown of the allocentric (exocentric) garding the PCC. spatial reference frame (Aguirre & D’Esposito, 1999) To elucidate the brain mechanisms underlying visual of personally familiar space. This possible role of the recognition of personally familiar objects and places, PCC in topographical memory is consistent with the re- with particular interest in the role of the PCC, we sults of the lesion studies in animals (Markowska, performed an event-related fMRI study using normal Olton, Murray, & Gaffan, 1989; Murray, Davidson, Gaffan, subjects. Four categories of stimuli, constituting a two- Olton, & Suomi, 1989; Sutherland, Whishaw, & Kolb, factorial design, were prepared individually for each 1988), and those of functional imaging studies on topo- subject (Figure 1) and subjects performed a familiar/ graphic navigation (Burgess, Maguire, Spiers, & O’Keefe, unfamiliar judgment during the fMRI experiment. Pic- 2001; Mellet et al., 2000; Ghaem et al., 1997; Maguire, tures for the familiar place (FP) category were taken in Frackowiak, & Frith, 1997). In contrast to the view of a places familiar to each subject in his/her daily life space-specific role of the PCC, however, a role in epi- (Figure 1A). Pictures for the familiar object (FO) cate- sodic retrieval in general has been suggested for this re- gory were taken from objects of each subject’s personal gion by previous neuropsychological reports (Maeshima belongings (Figure 1B). Pictures for the unfamiliar place et al., 2001; Yasuda, Watanabe, Tanaka, Tadashi, & (UP) and unfamiliar object (UO) categories were taken Akiguchi, 1997; Valenstein et al., 1987) and functional from unfamiliar places and objects, respectively, with

Figure 1. Experimental design. Examples of the visual stimuli used for each category are presented. Pictures were originally in color. (A) Familiar places (FP), (B) familiar objects (FO), (C) unfamiliar places (UP), (D) unfamiliar objects (UO).

184 Journal of Cognitive Neuroscience Volume 17, Number 2 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929053124956 by guest on 27 September 2021 equivalent semantic and visual character (Figure 1C in the left superior parietal cortex and middle temporal and D, respectively). The main effect of stimuli (places/ gyrus, and in the right . Converse- objects) contrasts the FP and UP (place) trials with the ly, significantly increased differential activations in the FO and UO (object) trials, which differentiates brain re- object trials relative to the place trials were observed gions that process a specific stimulus type (i.e., places bilaterally in the occipito-temporal junctions and intra- or objects, irrespective of familiarity). The main effect parietal sulci, in the right , and in the mid- of familiarity (familiar/unfamiliar) contrasts FP and FO callosal sulcus. (familiar) trials with the UP and UO (unfamiliar) trials, Because the mean reaction times were significantly which differentiates brain regions involved in processing longer in the place trials than in the object trials, both personally familiar places and objects. Regions differential neural activations in the place trials might Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/17/2/183/1757137/0898929053124956.pdf by guest on 18 May 2021 showing an interaction of stimuli and familiarity, in the be related to differential task difficulty possibly reflecting sense of increased activation in the FP compared to any differences in the visual complexity of the stimuli or in other stimulus categories, were assumed to be involved their retrieval. If this was the case, the results of the specifically in processing of personally familiar places. parametric analysis should show a significant positive As differences in task difficulty may exist across stimulus correlation between the reaction times and the ampli- categories, parametric analyses that evaluate the corre- tude of the cortical responses in both the place and lation between reaction times and the amplitude of cor- object categories. Such a significant correlation ( p < .05, tical responses were additionally performed to detect uncorrected) in both the place and object categories was any confounding effects of task difficulty. observed bilaterally in the posterior parahippocampal gyri and orbito-insular junctions, in the left PCC and superior occipital cortex, and in the right anterior RESULTS cingulate cortex. Inverse patterns, that is, a negative Behavioral data are shown in Table 1. Familiar/unfamiliar correlation in both the place and object trials, were categorization of each trial was based on each subject’s not observed in the areas showing differential neural response. Although each subject judged a few sup- activation in the object trials. posedly familiar stimuli as unfamiliar and/or a few sup- Areas showing a significant main effect of familiarity posedly unfamiliar stimuli as familiar, the mean numbers are given in Table 3 and Figure 3. Significant differential of trials in the four trial categories were balanced across neural activity in the familiar trials relative to the unfa- subjects. The mean reaction times were significantly miliar trials was observed in a posterior part of the right longer in the place trials than in the object trials both precuneus, the PCC with two discrete clusters, the left in the familiar and unfamiliar trials (paired t test, p < intraparietal sulcus, and bilaterally in the anterior cingu- .05). They were also significantly longer in the unfamiliar late cortices. No significant differential activation in the trials than in the familiar trials both in the place and unfamiliar trials compared with the familiar trials was object trials (paired t test, p < .05). The differences in observed. Although the mean reaction times were sig- the mean reaction times between familiar and unfamiliar nificantly longer in the unfamiliar trials than in the trials were not significantly different between the place familiar trials, no area showed a significant correlation and object trials. between the reaction time and the amplitude of cortical Areas showing a significant main effect of stimuli are response in both the familiar and unfamiliar trials. given in Table 2 and Figure 2. Significantly increased A significant interaction with greater activation in the differential activations in the place trials relative to the FP trials was observed in the right PCC only (Table 4 and object trials were observed in the posterior medial Figure 4). In this area, no significant difference in the cortices, including the parahippocampal gyri, the poste- activation pattern was observed between the FO and UO rior cingulate cortices, and the lingual gyri, bilaterally, trials, therefore, the differential activation in this area and the right precuneus. Additional activations were was specific for the FP trials. observed bilaterally in the superior occipital cortices, To illustrate the relationship of the four activated areas orbito-insular junctions and anterior cingulate cortices, in the PCC to anatomical landmarks, they are projected onto a single paramidsagittal plane (Figure 5A). The area with a significant effect of familiarity lying on the Table 1. Behavioral Data callosal sulcus immediately posterior to the splenium appears to correspond to the anatomically defined FP FO UP UO retrosplenial cortex (BA 26, 29, and 30) (Vogt, Vogt, No. of trials 26.1 ± 7.0 31.7 ± 2.7 33.9 ± 7.0 28.3 ± 2.7 Perl, & Hof, 2001; Brodmann, 1909). Concerning the rest Reaction time 1224 ± 247 888 ± 106 1324 ± 253 999 ± 123 of the PCC, its anatomical parcellation is controversial (msec) among existing anatomical maps, and its relationship to anatomical landmarks has often been unclear (Vogt, The number of trials categorized according to the subject’s response and the mean reaction times are shown for each of the four trial Vogt, et al., 2001; Sarkisov, Filimonoff, & Preobrashen- categories. The values given are the means ± standard deviations. skaya, 1949; von Economo & Koskinas, 1925; Vogt &

Sugiura et al. 185 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929053124956 by guest on 27 September 2021 Table 2. Areas Showing a Significant Main Effect of Stimuli

Correlation with the Reaction Times (t Value) Talairach Coordinate Cluster Size Structure (x, y, z) t Value (mm3) Place Object

Place > Object Posterior cingulate cortex L 14, 60, 22 18.94 78,992* 3.30 1.81 R8,54, 12 20.14 * 2.81 ns Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/17/2/183/1757137/0898929053124956.pdf by guest on 18 May 2021 Posterior L 24, 38, 16 18.89 * 1.83 2.05 R 26, 40, 14 13.95 * 2.09 2.03 Anterior parahippocampal gyrus L 24, 16, 22 5.11 * ns ns R 26, 16, 22 7.22 * ns ns Superior occipital cortex L 36, 76, 30 11.74 * 3.29 3.18 R 40, 80, 30 9.48 7416 ns ns L 12, 68, 58 5.78 1464 ns ns L 14, 92, 6 7.03 * ns ns R 26, 74, 8 6.19 * 2.08 ns Precuneus R 2, 46, 42 5.49 1160 ns ns L 52, 12, 14 7.27 840 ns ns Superior frontal sulcus R 30, 2, 44 8.73 1416 ns ns Orbito-insular junction L 32, 28, 10 6.80 1856 3.64 2.05 R 34, 26, 8 5.73 1448 3.58 5.80 Anterior cingulate cortex L 10, 20, 42 5.91 7840y 3.83 ns R 10, 12, 50 5.61 y 4.46 2.52

Object > Place Inferior occipito-temporal junction L 46, 60, 2 10.65 4592 ns 3.98 R 52, 70, 8 9.71 3120 1.85 1.98 Intraparietal sulcus L 52, 42, 48 7.14 4144 ns ns R 50, 36, 44 8.93 4088z ns ns Angular gyrus R 40, 62, 56 7.94 z ns 2.53 Mid-callosal sulcus M 2, 26, 22 7.57 1598 1.79 ns

The Talairach coordinates of the peak activation and the respective t values, as well as the size of the cluster (mm3) of the activated areas in the subtraction analysis are shown. The t values were thresholded at p < .001, and a correction for the multiple comparisons was performed by the cluster size level ( p < .05). Each of *, y, and z indicates that the activation peak is involved in the same cluster. The t values in the parametric analyses with the reaction times for the place trials (FP + UP) and object trials (FO + UO) at each voxel are also shown ( p < .05, uncorrected). Positive and negative values indicate positive and negative correlations, respectively. L = left; R = right; M = midline; ns = not significant ( p = .05).

Vogt, 1919; Brodmann, 1909). Accordingly, we refer to the to as the mid-dorsal posterior the remaining three areas as follows: the area with a cingulate cortex (mPCC). significant effect of stimuli adjacent to the occipito- parietal sulcus as the caudal posterior cingulate cortex (cPCC), that with the FP-trials specific activation adja- DISCUSSION cent to the splenial sulcus as the posterodorsal posterior cingulate cortex (pPCC), and that with a significant The most striking finding of our study is the differential effect of familiarity adjacent to the ascending limb of activation observed in a region in the PCC specifically in

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Figure 2. Areas showing a significant main effect of stimuli. (A) Areas showing greater activation in the place than object trials. (B) Areas showing greater activation in the object than place trials. In each panel, activations are presented using three glass brain representations of stereotactic space from the right, back, and top. Representative activated areas are superimposed on an appropriate slice of the mean normalized anatomical T1-weighted MRI of all subjects. Activation profile in the parameter estimates is also shown for each of these activation peaks.

the FP trials, suggesting an important role of this region functional specialization in the PCC in spatial and in the representation of personally familiar places. A nonspatial memories. significant main effect of familiarity with greater activa- tion in the familiar than unfamiliar trials was also observed in the PCC, as well as two other posterior Functional Subdivisions of the PCC cortical areas. The existence of discrete areas in the PCC each responding either to solely personally familiar The human PCC is composed of multiple anatomical places, or to both familiar places and objects suggests areas (Vogt, Vogt, et al., 2001; Sarkisov et al., 1949;

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Correlation with the Reaction Times (t Value) Talairach Coordinate Cluster Size Structure (x, y, z) t Value (mm3) Familiar Unfamiliar

Familiar > Unfamiliar Posterior precuneus L 4, 72, 36 8.57 9936* ns ns Posterior cingulate cortex M 0, 32, 42 7.54 * ns ns Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/17/2/183/1757137/0898929053124956.pdf by guest on 18 May 2021 L 2,40, 26 5.16 672y ns ns R6,44, 20 4.55 y ns ns Intraparietal sulcus L 50, 42, 46 6.16 2104 ns 2.22 Anterior cingulate cortex L 4, 36, 28 4.70 1104z ns 2.41 R 10, 24, 18 5.26 z ns 2.74

Unfamiliar > Familiar No significant activation

Presentation is in the same way as in Table 2 except that t values of the parametric analyses with the reaction times are shown for the familiar trials (FP + FO) and unfamiliar trials (UP + UO).

von Economo & Koskinas, 1925; Vogt & Vogt, 1919; explained by this mechanism when one of the tasks Brodmann, 1909). Inhomogeneous neuropsychological employed is more difficult than the other. Second, deficits reported for patients with posterior cingulate showing the activation peaks in previous functional lesions, for example, selective topographic memory imaging studies of emotion scattering over the entire deficits (Takahashi et al., 1997; Cammalleri et al., 1996) PCC, Maddock (1999) argued a major role of the PCC in or all-encompassing amnesia (Maeshima et al., 2001; emotional salience. Although the argument was criticized Yasuda et al., 1997; Valenstein et al., 1987), suggest the with respect to the anatomical definition and the direct existence of multiple functional subdivisions in this causality between emotional salience and the PCC acti- cortex. In monkeys, neurons involved in monitoring of vation (Maguire, 2001; Vogt, Absher, et al., 2000), it is eye movement were found in the cortex on the surface clear that differences in emotional salience may obscure of the cingulate gyrus superior to the splenium (Olson, any possible functional segregation of the PCC. We Musil, & Goldberg, 1996), but those related to sensory- reviewed activations in the PCC in previous functional triggered and self-paced forelimb movement were found imaging studies on episodic memory retrieval, excluding in the cortex buried in the cingulate sulcus (Shima et al., the results possibly explained by either task difficulty 1991); the two areas where these different populations (e.g., Grady, McIntosch, Beig, & Craik, 2001; Gorno- of neurons were found seem to be anatomically discrete Tempini et al., 1998) or emotional salience (e.g., Fink (Vogt, Finch, et al., 1992). et al., 1996). Not only the studies that explicitly re- The results of previous functional imaging studies are, quire retrieval of episodes, but also those in which the however, rather discouraging in terms of a putative tasks were likely to require retrieval of episodes, were functional segregation of this area in the ; included. We then found a segregation in the distribu- activation in the PCC has sporadically been reported in tion of the activation peaks when the tasks were divided many apparently unrelated cognitive domains with tre- by nature of the materials to be retrieved: whether it was mendous variability in locations (see Cabeza & Nyberg, experienced in real life or learned in the experimental 2000 for review). We point out two critical issues setting (Figure 5B and Table 5). concerning this controversy. First, it is known that the In a circumscribed area corresponding to the pPCC, PCC shows deactivation when any goal-directed task is activation was selective to tasks that require retrieval of compared with a ‘‘resting’’ state (Mazoyer, Zago, et al., materials experienced in real life, including retrieval of 2001; Shulman et al., 1997), and that the degree of this autobiographical events (Maguire & Frith, 2003; Piefke, task-induced deactivation depends on task difficulty Weiss, Zilles, Markowitsch, & Fink, 2003; Maguire & (McKiernan, Kaufman, Kucera-Thompson, & Binder, Mummery, 1999; Maguire, Frackowiack, et al., 1997; An- 2003; Mazoyer, Wicker, & Fonlupt, 2002). Although the dreasen et al., 1995), mental imagery of walking in mechanisms underlying this deactivation are still a matter personally familiar places (Mellet et al., 2000), and re- of debate, differential activations in the PCC may be trieval or judgment concerning familiar people or other

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Figure 3. Areas showing a significant main effect of familiarity with greater activation in the familiar than unfamiliar trials. Details are the same as in Figure 2.

real-world entity (Zysset, Huber, Samson, Ferstl, & von has a specific value to differentiate the materials. Al- Cramon, 2003; Kircher et al., 2002; Zysset, Huber, Ferstl, though the objects presented in our FO stimuli were & von Cramon, 2002; Leveroni et al., 2000). An event or also real-world entities, it is important to note that we item experienced in real life is usually woven into the carefully excluded objects that are associated with a nested linkage of other events and items to represent its specific place (see the Methods section). Thus, the meaning, and each event or item is usually associated assumed specific role of the pPCC in spatial representa- with specific places which carry a significant value to tion of personally familiar places is consistent with differentiate it from otherwise equivalent entities. On the previous functional imaging data. Neuropsychological contrary, materials learned in the experimental setting evidence (Maeshima et al., 2001; Takahashi et al., 1997; are usually encoded in a context where only their sensory Cammalleri et al., 1996) suggests that the spatial refer- feature and related semantic knowledge are meaningful, ence frame of the representation supported by this and the place where the learning was performed rarely region is allocentric (Aguirre & D’Esposito, 1999). In contrast, in an area corresponding to the mPCC, previously reported activations were predominantly in Table 4. An Area Showing Significant Interaction with tasks that required retrieval of experimentally learned Greater Activation in the FP Trials materials(Table5).Thedifferenceintheretrieved materials does not, however, explain the observed acti- Talairach vation pattern of the mPCC in this study. It should be Coordinate Cluster Size Structure (x, y, z) t Value (mm3) noted that all the tasks which activated the mPCC in the reviewed studies required quick responses by the sub- Posterior cingulate R2,52, 26 4.33 464 jects when they retrieved (Reber, Gitelman, Parrish, & cortex Mesulam, 2003; Reber, Wong, & Buxton, 2002; Burgess Presentation is in the same way as in Table 2. Correlation with the re- et al., 2001; Konishi, Wheeler, Donaldson, & Buckner, action times was not significant in all the trial categories. 2000; Henson, Rugg, Shallice, Josephs, et al., 1999;

Sugiura et al. 189 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929053124956 by guest on 27 September 2021 Figure 4. An area showing a significant interaction with greater activation in the FP trials. Details are the same as in Figure 2. Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/17/2/183/1757137/0898929053124956.pdf by guest on 18 May 2021

Buckner et al., 1996). The tasks in most of the studies navigation in large-scale space, and showed that the that did not report activation in the mPCC required majority of the activation peaks are located in the either no responses related to retrieval (Piefke et al., caudal part of the PCC corresponding to the cPCC. 2003; Shah et al., 2001), or responses based on higher- However, our review (Table 5 and Figure 5B) shows level cognitive operations based on the retrieved mate- that many episodic memory retrieval tasks on nonspa- rials (Maddock, Garrett, & Buonocore, 2001; Ryan et al., tial materials have activated also this area. Activation 2001; Mellet et al., 2000; Ghaem et al., 1997; Maguire, of this area was correlated with the reaction times in Frackowiak, et al., 1997; Andreasen et al., 1995). The the place trials in both the hemispheres and also in the mPCC may, therefore, act as an interface between object trials in the left hemisphere. Considering the episodic retrieval and motor response. It might be longer reaction times during the place than object trials, intriguing to compare the mPCC with the posterior part and, therefore, probably increased task difficulty, the of the cingulate sulcus in monkeys where the motor- cPCC is likely to be involved in effortful episodic related neurons were found (Shima et al., 1991). retrieval processes. The cPCC showed a significant effect of stimuli with Finally, concerning the retrosplenial cortex, a litera- greater activation in the place than object trials. Maguire ture review on the basis of Talairach coordinates appears (2001) reviewed previous functional imaging studies on not to be very helpful. Considering the fact that the

Figure 5. (A) Four activated areas in the PCC. Each activated area within 10 = x =10is projected onto the sagittal plane. The areas with a significant main effect of stimuli with greater activation in place than object trials (blue), those with a significant main effect of familiarity with greater activation in the familiar than unfamiliar trials (yellow), and those with a significant interaction with activation specific to the FP trials (red) are shown. The area with a significant main effect of stimuli with greater activation in place than object trials was thresholded at t-score = 12, and the remaining three areas at t = 3.79 ( p < .001, uncorrected for multiple comparison). (B) Activation peaks in the PCC in the reviewed studies on episodic retrieval are projected on the sagittal plane. An activation peak in a study using materials experienced in real life, and that in a study using materials learned in the experimental settings are shown as red circle and yellow triangle, respectively (see the legend of Table 5 for details). In both panels, areas or peaks are superimposed on the right parasagittal (x = 8 mm) slice of the mean normalized anatomical T1-weighted MRI of all subjects, as well as the schema of anatomical structures. CC = ; CallS = callosal sulcus; CiS = cingulate sulcus; SpS = splenial sulcus; OPS = occipito-parietal sulcus; CalcS = .

190 Journal of Cognitive Neuroscience Volume 17, Number 2 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929053124956 by guest on 27 September 2021 Table 5. Review of Posterior Cingulate Activation during Episodic Retrieval

Author ( Year) Contrast x y z

Retrieval of Materials Experienced in Real Life Andreasen et al. (1995) autobiographical episode–semantic memory 0 54 23 Maguire, Frackowiak, et al. (1997) route (in London) recall–number count 14 60 26 famous landmark recall–number count 14 52 20

Ghaem et al. (1997) mental navigation in real environment–rest 14 54 8 Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/17/2/183/1757137/0898929053124956.pdf by guest on 18 May 2021 mental navigation in real environment–rest 14 56 8 mental imagery of learned real building–rest 18 54 16 Craik et al. (1999) dispositional judgment on other–syllable counting 6 54 16 Maguire and Mummery (1999) autobiographical memory recall–control 4 56 24 Leveroni et al. (2000) famous face–unfamiliar face 2 53 29 8 45 7 famous face–learned face 4 57 15 2 57 29 Mellet et al. (2000) mental navigation in real environment–rest 16 56 12 mental navigation in real environment–mental map 12 46 28 Shah et al. (2001) familiar face/voice–unfamiliar face/voice 2 54 16 4 58 4 Sugiura et al. (2001) familiar face–dot location 2 53 16 familiar face–face direction 4 53 18 Simons et al. (2001) all face conditions (mostly famous)–all object conditions 2 57 21 Maddock et al. (2001) recall of familiar people by names–unfamiliar names 2 52 18 Ryan et al. (2001) autobiographical memory retrieval–rest/sentence 5to5 35 24 completion 10 55 15 14 55 15 Zysset, Huber, Ferstl, et al. (2002) evaluative judgment–semantic judgment 10 51 36 Kircher et al. (2002) self-descriptive (SD) personality trait–non-SD 12 22 31 6 53 31 6 53 37 Piefke et al. (2003) all autobiographical memory–baseline 6 56 4 recent event–far event 4 46 24 Zysset, Huber, Samson, et al. (2003) evaluative judgment–semantic judgment 3 47 28 Maguire and Frith (2003) autobiographical event–general knowledge (young) 3 60 27 autobiographical event–public event (young) 9 60 24 autobiographical event–autobiographical fact (young) 6 57 18 autobiographical event–public event (older) 6 57 24

Retrieval of Materials Learned in the Experimental Settings Tulving et al. (1996) old–new (learned picture/novel picture, odd ball task) 16 58 24 Buckner et al. (1996) recall–repetition (spoken words pair/picture–word pair) 3 37 28

(continued on next page)

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Author ( Year) Contrast x y z

Henson, Rugg, Shallice, Josephs, et al. (1999) recollection–new (word recognition) 6 24 27 6 42 36 recollection–know (word recognition) 0 30 36 Wiggs et al. (1999) episodic retrieval (object–color association)–object naming 4 38 16

4 38 16 Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/17/2/183/1757137/0898929053124956.pdf by guest on 18 May 2021 episodic retrieval (object–color association)–color naming 0 38 16 Konishi et al. (2000) hit–correct rejection (word recognition) 5 39 34 Henson, Rugg, Shallice, and Dolan (2000) old–new (word recognition) 3 42 21 Burgess et al. (2001) place context judgment–width judgment 15 60 18 6 30 30 person context judgment–width judgment 15 60 18 6 21 24 object judgment–width judgment 15 54 12 place context judgment–object judgment 12 48 6 9 45 6 18 33 39 3 33 42 person context judgment–object judgment 3 33 24 Maguire, Frith, and Cipolotti (2001) learned building recognition–control 20 58 16 Reber, Wong, et al. (2002) recognition–counting (dot pattern) 3 39 32 Fujii et al. (2002) time-context-specific recall–noun generation 9 55 12 person-context-specific recall–noun generation 4 55 12 Reber, Gitelman, et al. (2003) familiar dot pattern–unfamiliar dot pattern 12 34 46 4 27 34

Medial activation with a peak that satisfy the Talairach coordinate of 20 = x = 20, 60 = y = 20, and 0 = z = 50 was selected from contrasts likely reflecting episodic retrieval. Studies related to emotion and those that adopted a more difficult task in the control than in the task of interest were excluded (see text).

human retrosplenial cortex is mostly buried in the erality because it is sometimes difficult to determine callosal sulcus (Vogt, Vogt, et al., 2001; Brodmann, laterality of activation in medial structures (but see 1909), assignment of activations to the retrosplenial Maguire, 2001). When interpreting the results of the cortex seems to call for a revision in many previous current and previous functional imaging studies on functional imaging studies (see Vogt, Absher, et al., episodic retrieval, one should take into account differ- 2000). Results of a few studies presenting relatively ences in the period of memory retention between the reliable retrosplenial activation indicate that activation two types of materials. In the studies dealing with in this area is related to episodic memory retrieval (Shah materials experienced in real life, including our study, et al., 2001; Wiggs et al., 1999). Previous case reports experience has usually taken place weeks, months, or suggest that a lesion confined to the retrosplenial cortex years before the experiment. By contrast, in the studies can cause amnesia (Yasuda et al., 1997; Valenstein et al., dealing with materials learned in the experimental 1987). It thus appears that the retrosplenial cortex is setting, learning session was hardly ever performed involved in episodic memory retrieval, although its more than a few days before. This distinction would, precise role remains to be further elucidated. however, confound our results and conclusion only if As far as we know, this is a first attempt to show areas that showed a differential activation during famil- functional segregation in human PCC. We ignored lat- iar trials in this study had been selectively activated

192 Journal of Cognitive Neuroscience Volume 17, Number 2 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929053124956 by guest on 27 September 2021 during autobiographical retrieval tasks in previous stud- familiar trials. Activation of this area during successful ies, which was actually not observed. episodic memory retrieval has been shown in previous functional imaging studies (Henson, Rugg, Shallice, & Dolan, 2000; Konishi et al., 2000; Henson, Rugg, Shallice, Visual Recognition of Personally Familiar Objects Josephs, et al., 1999), although the primary role of this A significant main effect of stimuli with greater activa- region is yet to be reconciled among visual imagery tion in the object trials was observed bilaterally in the (Fletcher, Shallice, Frith, Frackowiak, & Dolan, 1996; inferior occipito-temporal junctions and intraparietal Fletcher, Shallice, Frith, Baker, et al., 1995), visuospatial sulci. Involvement of the inferior occipito-temporal attention (Corbetta, Shulman, Miezin, & Petersen, 1995; junctions in the visual shape or identity analysis in Corbetta, Miezin, Shulman, & Petersen, et al., 1993), and Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/17/2/183/1757137/0898929053124956.pdf by guest on 18 May 2021 object recognition has been established (Grill-Spector, episodic memory retrieval (Buckner et al., 1996; Fink Kushnir, Edelman, Avidan, et al., 1999; Grill-Spector, et al., 1996). Kushnir, Edelman, Itzchak, & Malach, 1998; Kanwisher, Taken together, following the visual processing in the Woods, Iacoboni, & Mazziotta, 1997; Malach et al., 1995; inferior occipito-temporal junction, and possibly in the Kosslyn et al., 1994). Although the scenes shown during intraparietal sulcus, successful recognition of personally the place trials also included objects, it is reasonable to familiar objects accompanies activation in the retrosple- assume that the subjects paid more attention to the nial cortex, mPCC, and precuneus, which appear to shape or identity of the objects during the object trials, support episodic retrieval, as well as the left intrapar- because subtle differences in the features of a single ob- ietal sulcus, which likely represents the experience ject were critical for each judgment. It has been shown of manipulation. that more attention to the shape or identity causes greater activation in the inferior occipito-temporal junc- Visual Recognition of Personally Familiar Places tions (Marois, Leung, & Gore, 2000; Ko¨hler, Kapur, Moscovitch, Winocur, & Houle, 1995). Although many cortical areas showed a significant main Activations in the intraparietal sulci were unexpected effect of stimuli with greater activation in the place trials, based on the results of previous studies on object the reaction-time data and the results of a parametric recognition. It is not likely that nonspecific visual atten- approach suggest that they can be explained by nonspe- tion explains this activation, considering the shorter cific effects of differences in task performance or task dif- reaction times in the object than place trials, and the ficulty. Therefore, we keep the discussion of these results fact that the activation appears specific to the object to a minimum. Many functional imaging studies have trials. An alternative explanation can be derived from shown activation in the parahippocampal gyrus during the fact that the personally familiar objects presented in visual processing of scenes and buildings (Epstein, our study were typically objects that subjects touched Graham, & Downing, 2003; Ko¨hler, Crane, & Milner, and handled in daily life. A behavioral study has sug- 2002; Gorno-Tempini & Price 2001; Nakamura et al., gested that behavior during object viewing is biased by a 2000; Epstein, Harris, et al., 1999; Aguirre, Zarahn, & motor program to manipulate the object without inten- D’Esposito, 1998; Epstein & Kanwisher, 1998), consistent tion of actual manipulation (Tucker & Ellis, 1998). A with our results. Involvement of the parahippocampal recent functional imaging study suggested that this gyrus in visual place processing is supported by reports sensorimotor transformation from object to action is of patients with lesions in medial occipito-temporal supported by a network including the intraparietal and regions manifesting landmark agnosia (McCarthy et al., inferior parietal cortex (Rumiati et al., 2004). This area is 1996; Habib & Sirigu, 1987; Landis et al., 1986). also activated during actual object manipulation The results suggest that successful recognition of (Grefkes, Weiss, Zilles, & Fink, 2002; Inoue et al., 2001; personally familiar places activates the pPCC, in addition Ja¨ncke, Kleinschmidt, Mirzazade, Shah, & Freund, 2001; to the areas involved in recognition of personally famil- Binkofski et al., 1999), or viewing of tools (Handy, iar objects. It is important to note that the patients with Grafton, Shroff, Ketay, & Gazzaniga, 2003; Chao & lesions in the pPCC or in its proximity do visually Martin, 2000). More attention to the feature of each recognize familiar places, but loose orientation there object during the object than place trials may thus have (Maeshima et al., 2001; Takahashi et al., 1997; Cammal- resulted in a differential activation of the motor repre- leri et al., 1996). Failure in scene recognition occurs in sentation of the object or its use. The left intraparietal patients with lesions in the medial occipito-temporal sulcus showed also a significant main effect of familiarity regions (McCarthy et al., 1996; Habib & Sirigu, 1987; with greater activation in the familiar trials, suggesting Landis et al., 1986; He´caen et al., 1980), where activation an additional role for this region in motor representa- was not sensitive to the familiarity of the places in this tion specific to personally familiar objects, that is, study. The medial occipito-temporal regions, arguably memory of an experience of manipulation. the parahippocampal gyrus, may support the visual The posterior precuneus also showed a significant representation of familiar places. Comparison of visual main effect of familiarity with greater activation in the input and existing visual representations on familiar

Sugiura et al. 193 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929053124956 by guest on 27 September 2021 places is carried out in a local neural network in the are considered to have a role in nonspatial episodic medial occipito-temporal regions, arguably the parahip- memory retrieval. Although the cPCC showed a signifi- pocampal gyrus, and successful matching between the cant effect of stimuli, existing knowledge suggests a role input and representation results in output to distant of this subdivision in retrieval effort. Successful recogni- areas supporting other representations and processes. It tion of both personally familiar objects and places is reasonable to assume that activation of the medial activated the mPCC, retrosplenial cortex, and posterior occipito-temporal regions predominantly reflects the precuneus, which appear to play a role in episodic former process, because the BOLD signal response in retrieval, as well as the left intraparietal sulcus, which a specific cortical area reflects the input and intracortical is likely to support memory of experiences concerning processing rather than the output (Logothetis, Pauls, manipulation of personally familiar objects. Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/17/2/183/1757137/0898929053124956.pdf by guest on 18 May 2021 Augath, Trinath, & Oeltermann, 2001). Personally familiar places can be represented not only in an allocentric but also in egocentric spatial reference METHODS frame. Impairment in representing the location of ob- jects with respect to the self is a feature of egocentric Subjects disorientation, and is observed in patients with lesions in Twenty-five healthy right-handed volunteers (20 men the bilateral or right posterior parietal cortex (Halligan, and 5 women, aged 18–31 years) participated in the Fink, Marshall, & Vallar, 2003; Vogeley & Fink, 2003; study. None had past histories of neurological or psy- Aguirre & D’Esposito, 1999). We assume involvement of chiatric illness. The handedness was evaluated using the left intraparietal sulcus in egocentric spatial repre- the Edinburgh Handedness Inventory (Oldfield, 1971). sentation of personally familiar places in addition to that Written informed consent was obtained from each sub- in motor representation of personally familiar objects, ject prior to participation in the study. The study was because both are related to motor coordination in approved by the local ethics committee. egocentric spatial reference frame. Stimuli and Tasks Future Perspectives A set of 120 individual stimuli was tailored for each A famous place, which one has viewed and learned (e.g., subject. In each stimulus category, pictures were taken in the TV or magazines), but where one has never been, in three different views for each of the 10 places/objects is another class of familiar places. It might be intriguing using a digital camera. Places for the FP category were to compare brain activation during scene recognition selected based on detailed interviews with each subject. between famous and personally familiar places. Differ- Typical places included the subject’s office, the subject’s ential involvement of spatial representation, that is, acti- house, the cafeteria where the subject has lunch every vation of the pPCC and intraparietal sulcus, is expected. day, and the train station a subject uses every day. A putative gender difference in the brain mechanism Objects for the FO category were provided by the sub- of the recognition of personally familiar places and ject him/herself. Typical objects included the subject’s objects is also of interest. In fact, a gender difference own bag, coffee cup, cellular phone, and bicycle. Objects in brain mechanisms of autobiographical retrieval has with close association to a specific place, such as the been suggested (M. Piefke, personal communication on desktop computer and kitchen wares, were excluded. Piefke et al., 2003). Our results are less convincing when Stimuli in the UP and UO categories were usually se- separating the female from the male population, most lected from those obtained as familiar stimuli for other likely due to the small number of women (n = 3) in our subjects, matching visual and semantic features to the study. However, we obtained a similar pattern of activa- familiar stimuli as much as possible. Visual stimuli were tion when the data of the male subjects (n = 12) only projected to the semilucent screen in front of the head were analyzed. coil of the MRI scanner, and each subject viewed them via a mirror. Each stimulus subtended a visual angle of approximately 108. Stimuli were presented for 0.5 sec Conclusions followed by an interstimulus interval with a random The data suggest the existence of four functional sub- duration (3.1 to 28.3 sec). All 120 stimuli were presented divisions in the human PCC, namely, the retrosplenial during a 906-sec span of trials. A random mosaic picture cortex, cPCC, pPCC, and mPCC, and a review of previous was presented during the interstimulus interval, and a functional imaging studies supports the concept of a central fixation cross was always presented. Each subject functional segregation put forward. The pPCC, which was required to keep the gaze at the fixation cross showed activation specific to the FP trials, is likely to during the fMRI measurement. The relatively short support allocentric spatial representations of personally stimulus presentation time was adopted based on the familiar places. The retrosplenial cortex and the mPCC results of a pilot experiment which showed that longer were sensitive to familiarity in both stimulus types, and presentation times made it difficult for the subjects to

194 Journal of Cognitive Neuroscience Volume 17, Number 2 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929053124956 by guest on 27 September 2021 maintain central fixation. Each subject was instructed to former was masked with FP–null, FO–null, FP–UP, and press a button as quickly as possible with the right index FO–UO, and the latter with UP–null, UO–null, UP–FP, finger when the presented place or object was familiar, and UO–FO. To extract regions showing a significant and another button with the right middle finger when it interaction between factors stimuli and familiarity, in a was unfamiliar. way that activation is selective to the FP trials, a contrast (FP UP)–(FO UO) was tested, and masked with FP– null, FP–FO, and FP–UP. Activation was thresholded at fMRI Measurement and Image Preprocessing p < .001 in the height, and corrected for multiple Thirty transaxial gradient-echo images (echo time = comparisons in the cluster size ( p < .05). The masks 66 msec, flip angle = 908, slice thickness = 3.5 mm, were applied at p < .05 without correction for multiple Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/17/2/183/1757137/0898929053124956.pdf by guest on 18 May 2021 slice gap = 0.35 mm, FOV = 200 mm, matrix = 64 64) comparisons. Search volume for the correction for covering the whole were acquired at a repe- multiple comparisons was the entire brain except for tition time of 3020 msec using the echo-planar sequence the activations in the PCC in the analyses exploring a on a Siemens Sonata (1.5T) (Siemens, Erlangen, Ger- significant main effect of familiarity and an interaction, many) scanner. Excluding the dummy scans for stabili- for which a box-shaped search area (20 = x = 20, zation of the T1 saturation effect, 300 volumes were 60 = y = 20, and 0 = z = 50, see Figure 5a and b) acquired during the task duration for each subject. An was used for a small volume correction. anatomical T1-weighted dataset (MP-RAGE) was also Parametric analysis to evaluate correlation between acquired after the experiment or on a separate occa- reaction times and the amplitude of cortical activations sion. The following preprocessing procedures were per- was performed using ‘‘parametric modulation’’ imple- formed using Statistical Parametric Mapping 99 (SPM99) mented in SPM99. This analysis is also a multiple regres- software (Wellcome Department of Imaging Neurosci- sion analysis, but it implements not only the canonical ence, London, UK) and MATLAB (Mathworks, Natick, model of the expected signal change, but also a model MA, USA): adjustment of acquisition timing across slices, of cortical responses with the same event timings but correction for head motion, coregistration to the ana- with the amplitude being correlated with the reaction tomical image, spatial normalization using the anatom- times for each of the four trial categories. The obtained ical image and the MNI template, and smoothing using parameter estimates for the models with modulated a gaussian kernel with a full width at half maximum of response amplitudes were tested across all the subjects 10 mm. Data from 10 subjects (7 men and 2 women) (random effects model) at each voxel of interest ( p < .05, with excessive head motion (more than 3 mm) and/or without correction for multiple comparisons). To test in dubious task performance (recognized less than 80% of the place, object, familiar, and unfamiliar trials, the supposedly familiar stimuli) were excluded from analy- parameter estimates for FP and UP, FO and UO, FP ses hereafter. and FO, and UP and UO, respectively, were averaged. Anatomical localization of the activations was per- formed by superimposing the activations onto the mean Statistical Analysis normalized anatomical T1-weighted MRI of all subjects. Trials were categorized into FP, UP, FO, and UO, accord- ing to the stimulus category (places/objects) and the Acknowledgments response of each subject (familiar/unfamiliar). The tim- ings for a ‘‘null events’’ were arbitrarily assigned. A con- We thank all the colleagues in the MRI and Cognitive ventional intrasubject event-related fMRI analysis of Neurology groups of the Forschungszentrum Ju¨lich for their support. MS is supported by the JSPS Postdoctoral Fellowships SPM99, that is, a multiple regression analysis imple- for Research Abroad (H.14). GRF and KZ are supported by the menting a model of expected BOLD signal changes for Deutsche Forschungsgemeinschft (DFG-KFO112). NJS, GRF, each of four trial categories and the null event, was per- and KZ are supported by the Bundesministerium fu¨r Bildung formed for each subject. Applying linear contrasts to the und Forschung (BMBF 01GO0104). obtained parameter estimates, effects of interest were Reprint requests should be sent to Dr. Motoaki Sugiura, tested across all the subjects (random effects model). Institut fu¨r Medizin, Forschungszentrum Ju¨lich, 52425 Ju¨lich, To extract areas showing a significant main effect of Germany, or via e-mail: [email protected]. stimuli, contrasts (FP + UP)–(FO + UO) (place > The data reported in this experiment have been deposited in object) and (FO + UO)–(FP + UP) (object > place) the fMRI Data Center (www.fmridc.org). The accession were tested; the former was masked with FP–null, UP– number is 2-2004-117G4. null, FP–FO, and UP–UO, and the latter with FO–null, UO–null, FO–FP, and UO–UP to assure that each was really an activation and a main effect. To extract areas REFERENCES showing a significant main effect of familiarity, (FP + Aguirre, G. K., & D’Esposito, M. (1999). Topographical FO)–(UP + UO) (familiar > unfamiliar) and (UP + UO)– disorientation: A synthesis and taxonomy. Brain, 122, (FP + FO) (unfamiliar > familiar) were tested; the 1613–1628.

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