Brain Imaging Group, Douglas Hospital Research Centre, Verdun, and Departments of Psychiatry and of Neurology and Neurosurgery, McGill University, Montreal, Québec, bec, Canada
Correspondence: Dr Martin Lepage, Douglas Hospital Research Centre - FBCI, 6875 Boulevard LaSalle, Verdun, Québbec ec H4H 1R3, Canada. Tel: +1 (514) 761 6131, ext. 4393; fax: +1 (514) 888 4064; e-mail: martin.lepage{at}mcgill.ca
Declaration of interest None. Funding detailed in Acknowledgements.
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ABSTRACT |
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Aims To identify in schizophrenia the brain regions in which activity is consistently abnormal across imaging studies of memory.
Method Data from 18 studies meeting the inclusion criteria were combined using a recently developed quantitative meta-analytic approach.
Results Regions of consistent differential activation between groups were observed in the left inferior prefrontal cortex, medial temporal cortex bilaterally, left cerebellum, and in other prefrontal and temporal lobe regions. Subsequent analyses explored memory encoding and retrieval separately and identified between-group differences in specific prefrontal and medial temporal lobe regions.
Conclusions Beneath the apparent heterogeneity of published findings on schizophrenia and memory, a consistent and robust pattern of group differences is observed as a function of memory processes.
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INTRODUCTION |
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METHOD |
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Data extraction and processing
Eighteen studies published between January 1996 and October 2004 met the
criteria for inclusion in our meta-analysis
(Table 1). Other studies
meeting our inclusion criteria except for the absence of Talairach/MNI
coordinates (Ragland et al,
1998; Shihabuddin et
al, 1998; Hazlett et al,
1999,
2000;
Nohara et al, 2000) were reviewed but were not included in the meta-analysis. Altogether, 228 foci
reported in these studies corresponded to a between-group difference in brain
activation during the performance of a memory task. Studies often used
different methods of analysis and different thresholds and so we included all
foci reported to be significant using the criteria designated in the
individual studies. Following a technique similar to that used by other groups
(Chein et al, 2002;
Turkeltaub et al,
2002; Wager et al,
2003,
2004), we created a
three-dimensional file with a value of 1 at each of these 228 foci and
smoothed it to model each focus as a Gaussian sphere with a full width at
half-maximum of 14 mm. After smoothing, the overlap of neighbouring Gaussian
spheres led to greater values, termed activation likelihood estimate (ALE)
values by Turkeltaub et al
(2002), in certain brain
regions where multiple foci agglomerated.
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Statistical significance of these ALE values was then determined using 1000 simulated sets of 228 randomly distributed foci throughout the brain. Based on these simulations, two methods were used to determine a significance threshold. First, following the method described by Turkeltaub et al (2002), we used as a threshold the ALE value that was observed with a voxel probability of 0.001 (i.e. obtained by chance only once in every 1000 voxels in the simulations). Second, we also extracted the value corresponding to 0.05 simulations (i.e. obtained by chance in at least 1 voxel in only 5% of the simulations). This threshold was found to be more restrictive than the voxel threshold and the regions that met this threshold are highlighted in bold characters in Tables 3 and 4.
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After applying this procedure for all 228 foci regardless of the tasks, we grouped the individual contrasts into independent categories:
Only two studies used contrasts that did not fit into any of these categories (see Table 1).
For the studies using high v. low levels of retrieval conditions, some between-group contrasts were performed using the within-group contrast in one direction (high retrieval > low retrieval), whereas others were in the other direction (low retrieval > high retrieval). To combine the different studies while taking the direction of the group difference into account, within-group contrasts that were in the low > high retrieval direction (Crespo-Facorro et al, 2001; Weiss et al, 2004) were reversed by also reversing the group comparison. (Between-group functional neuroimaging analyses are in fact group by task interactions, i.e. a contrast of contrasts. Within-subject contrasts have to be performed first and the output of these contrasts are then used for the between-group comparisons: it is a difference of differences. For two groups (A and B) and two tasks (1 and 2), we can say that mathematically (A1-A2)-(B1-B2)=(B2-B1)-(A2-A1) and (A2-A1)-(B2-B1)= (B1-B2)-(A1-A2). It is thus possible to reverse a within-subject contrast by also reversing the group contrast.) Three-dimensional maps of smoothed foci were then created and thresholded for each of the three categories and each between-group contrast direction (Table 2) with the same valid method that could also be used for combining within-group contrasts.
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RESULTS |
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Specific contrasts
The clustering into three categories allowed us to identify the regions
that were either more or less active in the schizophrenia group relative to
the control group.
For the encoding v. low-level baseline category (Table 4, Fig. 2a), the control group exhibited greater activation across studies in the left inferior prefrontal cortex, right anterior middle frontal gyrus, right medial frontal gyrus and right posterior hippocampus relative to people with schizophrenia. No region showed significant agglomeration for the schizophrenia group relative to controls.
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For the high retrieval v. low retrieval category (Table 4, Fig. 2c), a cluster of greater activation for the control participants was observed in the right posterior hippocampus. For participants with schizophrenia, clusters were observed in the cingulate gyrus, right parahippocampal gyrus and right superior parietal cortex.
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DISCUSSION |
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Left inferior prefrontal cortex
The left inferior prefrontal cortex was the main region that distinguished
between control and schizophrenia groups in this meta-analysis. This region
showed the most significant agglomeration of foci in the overall
meta-analysis, and was found to be consistently more active in controls
relative to people with schizophrenia during both encoding and retrieval
relative to baseline conditions. The region is involved in elaborative
semantic or phonological processing and in the implementation of strategies
(e.g. organisation) during episodic memory encoding
(Dempster & Brainerd,
1995; Simons & Spiers,
2003); it is also active during strategic search, the maintenance
of successfully retrieved information and response selection during retrieval
(Badre & Wagner, 2002; Petrides, 2002;
Petrides et al, 2002;
Simons & Spiers, 2003). Interestingly, it has been postulated that during encoding, people with
schizophrenia fail to engage spontaneously in efficient elaborative
processing. Ragland et al
(2001) have suggested that
people with schizophrenia process stimuli on a more superficial level and do
not spontaneously use semantic processing to guide memory encoding and
retrieval. None the less, it seems that people with schizophrenia can use
specific cues or strategies to improve their performance when they are
provided with them (Kubicki et
al, 2003; Ragland et
al, 2003). For example, Ragland et al
(2003) used a level of
processing paradigm (Craik & Lockhart,
1972) to study verbal recognition memory in schizophrenia. During
encoding, participants were instructed to make either upper case
v. lower case judgements (shallow encoding) or
concrete v. abstract judgements (deep
encoding). On a subsequent recognition memory test there was no significant
difference in performance between control participants and those with
schizophrenia, and both groups benefited from deeper encoding. Similarly, Paul
et al (2005) observed
a modulation of recognition memory performance by the level of processing in
schizophrenia, although in their study patients performed more poorly on the
recognition tasks relative to the control group. It follows that it is not
primarily the capacity to use elaborative processing to improve memory
performance that is affected in schizophrenia, but rather the tendency to use
a deep elaborative encoding strategy when no specific instructions are
provided.
In healthy participants a relationship between left inferior prefrontal cortex activity and the use of deeper processing during encoding has been extensively reported (e.g. Kapur et al, 1994; Kubicki et al, 2003; Petersson et al, 2003). This same relationship was examined in people with schizophrenia by Kubicki et al (2003), who contrasted the neural correlates of elaborative semantic processing with those related to perceptual processing. Relative to controls, people with schizophrenia showed reduced activation of the left inferior prefrontal cortex for the contrast between semantic and perceptual encoding, despite their normal performance and despite the normal modulation of memory performance by level of processing (Craik & Lockhart, 1972). This difference in activation may stem from a between-group difference in stimulus processing, reflecting either relatively reduced processing during semantic encoding or relatively increased processing during perceptual encoding, even if this difference does not affect subsequent recognition performance.
It has been suggested that some of the cognitive impairments in schizophrenia might be secondary to patients impaired ability to use organisational strategies to maximise performance (Bauman, 1971; Koh et al, 1976; Iddon et al, 1998; Hazlett et al, 2000). For instance, people with schizophrenia do not spontaneously use semantic clustering as a strategy to improve their memory performance (Gold et al, 1992; Paulsen et al, 1995; Brebion et al, 1997, 2004; Hazlett et al, 2000; Nohara et al, 2000). Organisational strategies are thought to rely at least in part on the left inferior prefrontal cortex during both encoding and retrieval (Fletcher et al, 1998; Wagner et al, 1999; Simons & Spiers, 2003). With regards to retrieval, Nohara et al (2000) have observed a significant correlation between categorical clustering and the activation in this cortical region in control participants that was not observed in people with schizophrenia. Taken together, these results suggest that the differential activation of this region in people with schizophrenia could be related to their inability to use efficient strategies spontaneously during both encoding and retrieval.
Another possibility is that the decreased activation of the left inferior prefrontal cortex is related to memory performance because this region has also been thought to be involved in retrieval success (Habib & Lepage, 2000; Konishi et al, 2000). The region was, however, observed to be deactivated in schizophrenia even when there was no significant difference in performance between groups (Andreasen et al, 1996; Wiser et al, 1998; Ragland et al, 2001; Hofer et al, 2003a; Kubicki et al, 2003). Even if it has been shown that people with schizophrenia are less likely to base their recognition judgements on conscious recollection relative to control participants (Huron et al, 1995; Danion et al, 1999), it is unlikely that the deactivation of this cortical region observed in this group relates to the reduced proportion of successfully or consciously recollected items, because there was no significant clustering of differential activation between groups in that region for the contrast between high and low retrieval conditions.
Medial temporal lobes
Functional neuroimaging studies in healthy individuals have consistently
implicated the medial temporal lobes in both memory encoding and memory
retrieval (Lepage et al,
1998; Schacter & Wagner,
1999). During encoding, the hippocampal formation is thought to
support the encoding of information in a meaningful way, such as creating new
associations (Vandenberghe et al,
1996; Henke et al,
1997,
1999;
Lepage et al, 2000;
Davachi et al, 2001; Davachi & Wagner, 2002;
Achim & Lepage,
2005b). Medial temporal activation during encoding has
also been shown to predict subsequent recognition success
(Brewer et al, 1998; Wagner et al, 1998;
Davachi et al, 2003;
Chua et al, 2004; Jackson & Schacter, 2004),
supporting the implication of this structure in the creation of durable memory
traces. Our meta-analysis revealed a significant agglomeration of foci of
reduced activation in people with schizophrenia in the right hippocampus
during encoding, possibly reflecting the less efficient or less associative
encoding strategies used by people with schizophrenia.
Different lines of evidence suggest that during memory retrieval the hippocampus supports conscious recollection of information from memory, whereas the parahippocampal gyrus is involved in familiarity assessment (Yonelinas, 2002). It has also been suggested that people with schizophrenia could have a specific deficit in conscious recollection (Huron et al, 1995; Danion et al, 1999; Weiss et al, 2003). The results from our meta-analysis support this idea by showing that people with schizophrenia present a deactivation of the region implicated in conscious recollection (i.e. the hippocampus) when exposed to conditions favouring the recovery of information from memory (high v. low retrieval). Moreover, this hippocampal deactivation is accompanied by an overactivation of the region implicated in familiarity assessment (i.e. the parahippocampal gyrus), suggesting that people with schizophrenia use familiarity assessment rather than conscious recollection as a basis for retrieval.
Another interesting observation is a focus of agglomeration of greater activation in schizophrenia relative to controls during memory retrieval v. baseline, centred in the right anterior medial temporal lobe. In contrast, control participants show greater left lateralised activation in this region for the same comparison. This pattern of activation is consistent with the idea that people with schizophrenia show less lateralised medial temporal activation as a function of stimulus type (verbal and non-verbal) (Crow et al, 1989; Gur et al, 1994), because all studies included in the retrieval v. baseline category used verbal stimuli.
Other frontal regions
A few other prefrontal regions showed significant agglomeration of foci in
our meta-analysis. For instance, the left middle frontal gyrus showed
significant agglomeration of foci in the controls relative to people with
schizophrenia for the retrieval v. baseline contrast. This region is
known to support post-retrieval monitoring during episodic memory retrieval,
with activation typically in the right middle frontal gyrus for more simple
monitoring and additional involvement of the left middle frontal gyrus for
more complex tasks (Achim & Lepage,
2005a). The observation that the left middle frontal
gyrus shows a greater activation in controls suggests a specific impairment of
more complex post-retrieval monitoring processes in schizophrenia, a view
consistent with the finding that more complex tasks reveal greater memory
impairment (Danion et al,
1999).
The anterior medial prefrontal cortex also showed significant agglomeration in the general meta-analysis as well as in encoding v. baseline and retrieval v. baseline. This region is thought to be involved in the retrieval of self-relevant or self-generatedgenerated self-information (Simons & Spiers, 2003; Fossati et al, 2004), although the specific mechanisms remain to be understood. Failure to activate these regions in people with schizophrenia could reflect their difficulty in using sources of information other than the ones provided by the task.
The anterior cingulate also showed significant agglomeration in both the overall meta-analysis and the high v. low retrieval category. Paus et al (1998) have suggested that the anterior cingulate has a role in memory and cognitive effort. It could be the case that this activity reflects the greater effort needed by people with schizophrenia to perform these memory tasks.
Other regions: cerebellum, thalamus
The cerebellum projects to motor and prefrontal regions of the cerebral
cortex through synapses in the thalamus. Through this circuit, the cerebellum
is thought to modulate and coordinate both motor and cognitive functions
(Andreasen et al,
1996,
1998,
1999). Converging evidence has
pointed to dysfunctions of this cortical-cerebellar-thalamic-cortical circuit
in schizophrenia, and our findings of significant agglomerations of foci
observed in the cerebellum and thalamus are consistent with this notion. The
specific neural mechanisms underlying the coordination of cognitive activity
by the cerebellum, however, remain to be clarified. It has been proposed that
the cerebellum could modulate memory processing through a mechanism for
correction of discrepancies (Schmahmann,
1991; Fink et al,
1996; Greve et al,
1999) or through a mechanism for coordination between different
pieces of information (Fabbro,
2000).
Studies without Talairach/MNI coordinates
Five functional neuroimaging studies of memory in schizophrenia could not
be included in the meta-analysis because no Talairach/MNI coordinates were
reported (Ragland et al,
1998; Shihabuddin et
al, 1998; Hazlett et al,
1999,
2000;
Nohara et al, 2000).
Two of these studies used restricted regions of interest either in the
thalamus (Hazlett et al,
1999) or in the striatum
(Shihabuddin et al,
1998) and observed decreased activation in these regions in
schizophrenia relative to controls. The other three studies examined the
entire brain and, consistent with our results, reported reduced activation in
participants with schizophrenia in the left inferior frontal gyrus and other
frontal regions (Ragland et al,
1998; Hazlett et al,
2000; Nohara et al,
2000) as well as in the temporal lobe
(Ragland et al, 1998;
Hazlett et al, 2000) during episodic memory tasks. Overall these results are consistent with those
that reported Talairach/MNI coordinates for peaks of activation, making it
unlikely that the exclusion of these five studies from our meta-analysis
biased our results.
Future research
In summary, the quantitative aspect of this meta-analytic method represents
an improvement over current qualitative methods because it offers an objective
way of regrouping studies and summarising results. However, it must be noted
that most of the studies reviewed here compared a memory task (encoding or
retrieval) with a low-level baseline. Such contrasts are not ideal for
discriminating the neural correlates of specific memory processes and instead
are likely to reflect several cognitive and perceptual processes
(Stark & Squire, 2001).
More sophisticated experimental designs would increase our chances of
identifying selective deficient processes in schizophrenia and ultimately the
neural correlates of these abnormal processes.
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Clinical Implications and Limitations |
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LIMITATIONS
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ACKNOWLEDGMENTS |
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Received for publication January 14, 2005. Revision received March 21, 2005. Accepted for publication March 29, 2005.
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