Preoperative Prediction of Verbal Episodic Memory Outcome Using fMRI

This article focuses on an important neurosurgical problem for which functional imaging may have a role. Temporal lobe epilepsy surgery typically involves removal of much of the anterior medial temporal lobe, which is critical for encoding and retrieval of long-term episodic memories. Verbal episodic memory decline after left anterior temporal lobe resection occurs in 30% to 60% of such patients. Recent studies show that preoperative fMRI can predict the degree of verbal memory change that will occur, and that fMRI improves prediction accuracy when combined with other routine tests. The predictive power of fMRI appears to be at least as good as the Wada memory test, making fMRI a viable noninvasive alternative to the Wada for preoperative assessment.

Interest in functional imaging of memory systems stems from 2 clinical problems. The first of these is localization of seizure foci in temporal lobe epilepsy (TLE). TLE often arises from the medial temporal lobe (MTL), and structural and functional abnormalities in the MTL can provide important evidence regarding seizure localization. Asymmetric sclerosis and volume loss in TLE can be detected with good sensitivity and specificity using structural MRI. Positron emission tomography (PET) may reveal interictal MTL hypometabolism and associated hypoperfusion in patients with TLE. The memory portion of the Wada test, which assesses episodic encoding during unilateral cerebral anesthesia, can detect asymmetric dysfunction of the MTL, which can be used to infer the laterality of a seizure focus. One potential application of fMRI, therefore, is to provide evidence about seizure focus laterality by measuring asymmetry of activation in the MTL. In addition to assisting in seizure focus identification, asymmetry of activation might be useful for predicting seizure outcome after anterior temporal lobe (ATL) surgery. When functional asymmetry consistent with the side of seizure focus is demonstrated on PET or on the Wada memory test, for example, seizure control is better than when no asymmetry or reversed asymmetry is observed. Although several fMRI studies suggest that MTL activation asymmetry may be correlated with side of seizure focus and seizure outcome in TLE, sample sizes in these studies have been small, and no studies have yet examined whether fMRI contributes additional predictive value beyond ictal EEG, ictal semiology, and structural MRI.

The present article focuses on an equally important neurosurgical problem for which functional imaging may have a role. Temporal lobe epilepsy surgery typically involves removal of much of the anterior MTL, including portions of the hippocampus and parahippocampus, which are known to be critical for encoding and retrieval of long-term episodic memories. Verbal episodic memory decline after left ATL resection is a consistent finding in group studies and is observed in 30% to 60% of such patients. In contrast, nonverbal memory decline after right ATL resection is less consistently observed in both groups and individuals. One main focus of the preoperative evaluation in ATL surgery candidates is, therefore, to estimate risk of verbal memory decline, particularly in patients undergoing left ATL resection.

The Wada memory test was originally developed for the purpose of predicting global amnesia after ATL resection, although its reliability for this purpose has often been questioned. Studies of its ability to predict relative verbal memory decline have been inconsistent, with several suggesting good predictive value and others showing little or none, particularly when used in combination with noninvasive tests. Other presurgical tests of MTL functional or anatomic asymmetry are modestly predictive of memory outcome, including structural MRI of the hippocampus and interictal PET. Preoperative neuropsychological testing also has predictive value, in that patients with good memory abilities before surgery are more likely to decline than patients with poor preoperative memory. Given the availability of these other known predictors, the value of fMRI depends not only on its ability to predict memory outcome in isolation, but also on its ability to contribute additional predictive value beyond other noninvasive measures.

A key point often neglected in discussion of these topics is that the goals of seizure focus lateralization and memory outcome prediction call for fundamentally different methodological considerations. In the case of seizure focus lateralization, the ideal fMRI procedure is probably one that activates the MTL symmetrically in healthy people, thus allowing optimal detection of deviation from normal symmetry in either direction. In contrast, prediction of verbal memory outcome requires an fMRI procedure that specifically identifies verbal memory processes. Because many stimuli are encoded into memory in both verbal and nonverbal forms, MTL activation resulting from such stimuli cannot be assumed to represent verbal memory processes. Stimuli that are dually encoded, such as pictures, might be ideal for producing bilateral MTL activation and thus for detecting seizure focus lateralization, whereas these same activation patterns, because they represent a mix of verbal and nonverbal processes, may predict little or nothing about verbal memory outcome.

Varieties of memory

Memory refers to the ability to store and retrieve information. The human brain performs 4 essentially different kinds of memory processes, distinguished by the type of information stored and the length of time over which storage persists. At one end of the spectrum is procedural memory , which refers to knowing how to do motor and sensory tasks. Common examples include walking, eating, throwing a ball, tying a tie, and riding a bike. The information stored involves complex sensory-motor sequences that are largely outside conscious awareness and cannot be described in detail. Another notable example of procedural memory is talking, which involves very complex sequences of tongue, lip, vocal cord, and diaphragm movements of which perfectly fluent speakers are largely unaware. Semantic memory refers to knowing facts about the world, such as the color of a banana, the capital of France, or the meaning of a word. Semantic memory allows us to recognize and name objects, produce and comprehend sentences, form opinions, and plan the future. Like procedural memory, information in semantic memory typically persists over an entire lifetime, although loss of semantic memory is a characteristic feature of some forms of dementia. At the other end of the spectrum, short-term memory refers to the ability to hold information in consciousness for seconds or a few minutes, usually by active mental recitation. Short-term memory allows us to hold in mind otherwise meaningless sequences like telephone numbers long enough to complete a task for which they are needed. The transient nature of short-term memory is illustrated by the fact that distraction of attention typically causes the information to rapidly fade, and by the common use of semantic memory in the form of “mnemonic devices” to allow longer maintenance of otherwise meaningless sequences.

The focus of the present review is episodic memory , which refers to the ability to update and maintain a conscious record of personal experiences. Episodic memory can include both verbal and nonverbal information, such as the content of recent conversations, names of new friends, personally experienced events and their order of occurrence, or the location of one’s car in a parking lot. Information in episodic memory can persist for hours, days, or years depending on factors such as the meaningfulness or emotional significance of the event and the frequency with which the event is recalled. Episodic memory was first linked conclusively with the MTL after cases of severe episodic memory loss, labeled amnesia, were reported from temporal lobe damage involving the MTL bilaterally. Such patients are unable to form new memories of events or learn new verbal information (anterograde amnesia), and may also lose partial memory of events experienced before the MTL damage (retrograde amnesia). In contrast, knowledge about objects and previously learned facts about the world are spared, as are motor skills and the ability to hold information through active recitation, indicating relative preservation of semantic, procedural, and short-term memory.

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