The auditory and association cortex and language evaluation methods

Handbook of Clinical Neurology, Vol. 160 (3rd series) Clinical Neurophysiology: Basis and Technical Aspects K.H. Levin and P. Chauvel, Editors https://doi.org/10.1016/B978-0-444-64032-1.00031-X Copyright © 2019 Elsevier B.V. All rights reserved

Chapter 31

The auditory and association cortex and language evaluation methods 1

ANDREW C. PAPANICOLAOU1,2*, ROOZBEH REZAIE1,2, AND PANAGIOTIS G. SIMOS3 Department of Pediatrics, Division of Clinical Neurosciences, University of Tennessee Health Science Center, Memphis, TN, United States 2

Neuroscience Institute Le Bonheur Children’s Hospital, Memphis, TN, United States

3

Department of Psychiatry & Behavioral Sciences, School of Medicine, University of Crete and Institute of Computer Science, Foundation for Research and Technology, Heraklion, Greece

Abstract This chapter presents a summary of current notions regarding cortical specialization for language and a description of the methods employed for the assessment of that specialization. We distinguish between the “canonical” model of language specialization as it evolved from the early observations of Broca and Wernicke, implicating the inferior frontal gyrus and the posterior temporal cortex of the speech dominant hemisphere (usually the left) and its modern variants that are based on both detailed studies of lesion-symptom correlations and on the results of functional brain mapping methods. The latter fall into two categories. The first includes the invasive ones, namely the Wada procedure for assessing hemispheric dominance for speech and cortical stimulation mapping (whether intraoperative or extraoperative) for identifying cortical nodes or “hubs” of the neuronal network for language. The second category includes the noninvasive methods of functional magnetic resonance imaging, magnetoencephalography, and transcranial magnetic stimulation used for both assessment of hemispheric dominance for language and for localization of the cortical nodes of the language network. The advantages and the shortcomings of all methods are juxtaposed to facilitate selection of particular methods of assessment of the locus of the language network in particular cases.

CURRENT OPINIONS REGARDING THE CORTICAL ORGANIZATION OF LANGUAGE The auditory and the temporal association cortex, as well as parts of the parietal and frontal cortices, are implicated in language production and perception functions. The cerebral hemisphere that is “dominant” for these two functions, and the precise location of the hubs of the neuronal networks that mediate them, are of central importance in the presurgical evaluation of many

epilepsy and tumor patients. There are two reasons presurgical language assessment is desirable: first, the individual variability in the precise locus of language-related cortical patches; and second, the well-attested additional variability resulting from cortical functional reorganization in the presence of lesions, especially slowly developing ones. The evaluation is pursued by means of invasive and noninvasive brain mapping methods. The essential features of these methods will be described, and their relative advantages and shortcomings will be commented on. Moreover, current opinions regarding

*Correspondence to: Andrew C. Papanicolaou, Ph.D., Professor, Department of Pediatrics, Division of Clinical Neurosciences, University of Tennessee Health Science Center, Memphis, TN 38105, United States; Co-director, Neuroscience Institute, Le Bonheur Children’s Hospital, 49 N. Dunlap street, 3rd floor, Memphis, TN 38105, United States. Tel: +1-901-287-5638, Fax: +1-901-287-5385, E-mail: [email protected]

466

A.C. PAPANICOLAOU ET AL.

the role of the different cortical regions in particular aspects or subsidiary operations of the speech production and perception functions will be summarized. Several different hypotheses as to the precise nature of specialization of each cortical region for specific aspects of linguistic processing have emerged over the years, from observation of the effects of focal lesions and, more recently, from functional neuroimaging data. These differ because the lesion data are rarely sufficiently clear to support a particular hypothesis unequivocally, since lesions vary across patients in severity, extent, and other aspects, and because the interpretation of more recent functional neuroimaging data is hampered by a number of unresolved technical problems. Although there is very little agreement regarding which cortical regions are necessary for what specific linguistic operations, some exceptions do exist. First, it is universally acknowledged that acoustic processing of both speech and nonspeech stimuli is mediated by the auditory cortex in the midportion of the superior temporal gyrus (STG) in the left and right hemispheres equally. Second, it is acknowledged that the inferior frontal gyrus (IFG), comprising pars opercularis and pars triangularis, is necessary for production of speech in general. There is also considerable agreement that IFG may be necessary for comprehension of sentences, that is, for syntactic processing of linguistic input, though its contribution is not necessary for comprehension of isolated words (Mesulam et al., 2015). Beyond these points of agreement, most other hypotheses regarding cortical organization for language vary among theorists. According to the “canonical” model that has emerged over the years, mostly from consideration of the effects of focal cortical lesions, phonological processing of linguistic input requires the contribution of the posterior part of STG (pSTG) of only the left hemisphere (Wernicke, 1874/1969; Luria, 1970; Scott et al., 2000; Rauschecker and Scott, 2009). This view has been recently challenged, however, especially by Hickok and Poeppel (2000, 2007, 2015) on the basis of results of some focal lesion studies (Miceli et al., 1980; Buchman et al., 1986; Rogalsky et al., 2008; Rogalsky and Hickok, 2011) and of some functional neuroimaging data (Turkeltaub and Coslett, 2010; Price, 2012; Schirmer et al., 2012). They have proposed a “dual-route” model, which predicts that in tasks requiring perception of speech sounds both the left and the right pSTG are active, although the contribution of the anterior STG cannot be ruled out (see, e.g., Scott et al., 2000; Narain et al., 2003; Spitsyna et al., 2006). On the basis of this model, it is further expected that electrical stimulation in either the left or the right pSTG (and/or the anterior STG) would not result in interference with phonemic perception, based on lesion data suggesting that the unaffected STG of either hemisphere should suffice in mediating phoneme

perception tasks (Miceli et al., 1980; Buchman et al., 1986; Rogalsky et al., 2008; Rogalsky and Hickok, 2011). With respect to semantic processing required for comprehension of individual words, the canonical view since the time of Wernicke’s first publication on this issue (Wernicke, 1874/1969) is that this linguistic operation is mediated by the region that encompasses pSTG, a portion of the middle temporal gyrus, and the angular and supramarginal gyri of the left cerebral hemisphere in most people. This view has been widely supported by clinical data indicating that lesions in that area appear to disrupt comprehension of both words and sentences (Marie, 1906; Lhermitte and Gautier, 1969; Geschwind, 1972; Bogen and Bogen, 1976; Naeser et al., 1987; Turken and Dronkers, 2011). But this view has also been challenged by dementia data (Snowden et al., 1989; Hodges et al., 1992; Rogers et al., 2004; Jefferies and Lambon Ralph, 2006; Patterson et al., 2007; Hurley et al., 2012; Mesulam et al., 2013) and focal lesion data (Schwartz et al., 2009), indicating that, whereas Wernicke’s area, as defined previously, may appear to be necessary for both phonological and semantic analyses of linguistic input, it is actually necessary for phonological analysis only, resulting in the derivation of the word form (i.e., an activation pattern coding the phonological profile of words; see, e.g., Pulvermuller and Fadiga, 2010; Pulvermuller, 2013). However, in the context of this alternative view, its disruption would be expected to affect not only phonological analyses but also interfere with word and sentence comprehension, because the latter presuppose phonological analysis and not because the area mediates semantic operations. The latter, according to this alternative view, are mediated by the left anterior temporal lobe (ATL) instead, but the precise role of ATL is not clear. According to one hypothesis (Mesulam et al., 2015), ATL is necessary for mediating the activation of semantic circuits distributed throughout the cortex on the basis of word formrelated input that it receives from Wernicke’s region, or for activating word form circuits on the basis of input from semantic circuits as in object naming tasks (Schwartz et al., 2009; Mesulam et al., 2013). Therefore, according to this alternative to the canonical model, disruption of the left ATL by electrical stimulation would be expected to interfere with word comprehension (consequently also sentence comprehension) tasks and/or performance of object naming tasks, whereas increased activation during word comprehension tasks should be found in both the left ATL and Wernicke’s area, especially the pSTG. But the results of some cortical stimulation mapping (CSM) studies (Luders et al., 1986) have pointed to the conclusion that the left fusiform gyrus (rather than the left ATL) is necessary for word and sentence comprehension, leading to the expectation

THE AUDITORY AND ASSOCIATION CORTEX

467

Fig. 31.1. Sites in the left hemisphere leading to interference (D) with speech and to speech arrest (A) following electrical stimulation. Adapted from Penfield W, Roberts L (1959). Speech and brain mechanisms. Princeton University Press; Princeton, NJ, US.

that during word and sentence comprehension tasks increased activation should be observed in this region. In view of the fact that most words used in that study were concrete nouns and in view of the known involvement of this area in object recognition, its contribution to word comprehension may be limited to that word category and to sentences that contain names of objects. On the basis of yet another lesion dataset (GornoTempini et al., 2004), it has also been proposed that word comprehension is mediated by the inferior temporal region and ATL bilaterally. These data, incorporated into the rationale of the “dual route” model, lead to the expectation that during word comprehension tasks, these areas rather than only the left ATL or the left Wernicke’s region should show increased activation (Hickok and Poeppel, 2015). As mentioned earlier, there is general agreement on the role of the left IFG in production of speech (whether of phonemes, words, or sentences) and in the comprehension of sentences. It is, however, disputed whether it suffices for the latter task since, according to the dual route model, cortex in the parieto-temporal junction covering the ventral bank of the left Sylvian sulcus (Spt) is necessary, along with IFG (pars opercularis), for the production of all sorts of structured sounds, from melodies to speech syllables to words and sentences (Hickok and Poeppel, 2015). This notion is supported by functional neuroimaging data (Hickok et al., 2003; Buchsbaum et al., 2005; Buchsbaum et al., 2011), as well as by the observation that conduction aphasia in patients displaying good word comprehension but frequent phonemic errors (Damasio and Damasion, 1980; Goodglass, 1993; Baldo et al., 2008) very often results from focal lesions encompassing Spt. It appears that each of the aforementioned cortical regions makes some contribution to language, since CSM results appear to implicate them all, as is evident from the composite map of language-related cortical topography shown in Fig. 31.1.

Although it would be theoretically desirable and of considerable practical significance to know exactly which particular linguistic operation is interfered with by the electrical stimulation in each of these cortical patches, such information is not yet available. Yet the fact that any of them is disrupted is a useful component of the planning of resections. The procedure through which the preceding topographical data are derived, along with the procedure for assessing hemispheric dominance for language, is described in the following section.

THE INVASIVE LANGUAGE ASSESSMENT PROCEDURES Determination of the language-related regions, as well as the somatosensory and motor cortex, and their relation to the diseased brain regions to be surgically removed is accomplished using two invasive procedures. The first is the intracarotid sodium amytal method, also known as the Wada test. The second is CSM performed intraoperatively, or in some cases extraoperatively through electrode arrays (grids or strips) placed below the dura mater for the primary purpose of estimating the location of the sources of epileptiform activity for subsequent resection. This method requires craniotomy and exposure of the cortex to be explored and the cooperation of the conscious patient (usually under light sedation). The former method addresses the question of hemispheric dominance for language and memory and the latter the localization of the expressive and receptive language-specific cortex, as well as that of the primary somatosensory and motor cortex. Both CSM and the Wada method are used to produce “reversible lesions” with the intention of selectively interrupting each of the previously named functions such that the location and extent of the brain circuitry mediating them may be identified. In the case of the Wada test, the lesion involves extensive sectors of each cerebral

468

A.C. PAPANICOLAOU ET AL.

hemisphere, mainly the regions irrigated by the anterior and middle cerebral arteries. In the case of CSM, the reversible lesions involve patches of the exposed cortex, approximately 1–2 cm in diameter. Provided that a reversible lesion impedes a particular function reliably, one can safely conclude that the tissue “lesioned” is a necessary component of the brain mechanism of the temporarily disrupted function. For that reason, both of these methods are often thought of as providing the “gold standard” for functional brain mapping.

The Wada procedure Typically, the Wada procedure involves the following steps (e.g., Loring et al., 1990): Intracarotid artery injections of sodium amobarbital are administered by hand during a 4–5s interval via a catheter, in the femoral artery. Patients are generally given an initial bolus of sodium amobarbital that varies between 75 and 125 mg, depending on their weight, followed by incremental injections of 12.5 mg, as needed to produce contralateral hemiplegia. Then, the patient’s comprehension of simple instructions (e.g., “stick out your tongue”) is tested. Subsequently, the testing for determining hemispheric dominance for language is initiated. This consists of: (1) testing for comprehension of one- and two-step commands (the most complex being commands involving inverted syntax), (2) naming of objects or parts of objects presented visually, (3) reading of sentences, and (4) repetition of simple phrases. Performance on each of these tests is scored as either normal or mildly, moderately, or severely deficient. An identical procedure is repeated in the other hemisphere after an approximately 30-min interval. Hemispheric dominance for memory is determined by asking the patient to recall or recognize items presented visually before language testing begins.

In order to assess receptive language, the train of electrical pulses is applied at the beginning of oral presentation of sentences; to assess expressive language, stimulation is initiated immediately after sentence presentation. In either case, interruption of receptive or expressive language is inferred if the patient has difficulty in responding appropriately to or repeating the sentences, respectively. Positive results (i.e., disruptions) are always verified by repeating stimulation at the same site at least twice and by assessing performance in the absence of stimulation. For intraoperative CSM, following exposure of the cortex, under local anesthesia and with the patient awake, electrical stimulation is applied using, typically, an Ojemann Stimulator (Integra NeuroSciences, Plainsboro, NJ). Stimulation is performed using 3–5-s long trains of square-wave pulses, again at a rate of 50 pulses per second (see Fig. 31.2). Concurrent recordings are obtained from the cortical surface using multicontact subdural strip electrodes. Current intensity is gradually increased while attention is paid to detect any after discharges on the ECoG. Systematic stimulation of the exposed cortex is then performed at the highest current intensity that does not result in after discharges. Specifically, language function is typically evaluated using three tasks: repetition of spoken sentences, comprehension of spoken sentences, and confrontation naming (i.e., naming objects and actions depicted in drawings of computer-generated images presented to the patient). Stimulation-induced interruption of the patient’s performance is defined as any error or as a significant increase in response time. Stimulation and no stimulation trials are randomly mixed, and several errors are required in order for a stimulation site to be considered part of the language mechanism. The set of all such sites circumscribes the CSM-derived functional map for language.

ECoG recordings The CSM procedure Extraoperative CSM is performed using multielectrode subdural strips or grids consisting of platinum disk electrodes 1 cm in diameter embedded in a plastic sheath, placed 1 cm apart. A pair of adjacent electrodes is connected to the output terminals of a stimulator and placed on the exposed cortical surface at locations selected in sequence to evaluate the entire exposed cortical surface. Electrical stimulation is typically performed using a 5-s train of square-wave pulses (at 500 ms per phase with a repetition rate of 50 pulses per second). For each pair of contacts, the stimulating current typically varies from 5.0 to 17.5 mA until either the function of interest is interrupted or abnormal discharges are observed in electroencephalographic recordings from the exposed cortex (electrocorticogram or ECoG), indicating that higher stimulation intensity is unsafe.

A rapidly growing alternative method to determine cortical sites involved in language functions involves analysis of stimulus-locked changes in high-frequency rhythmic activity (typically in the gamma range of 50–120 Hz). Commonly used tasks include sentence repetition (Wang et al., 2016) and object naming (Babajani-Feremi et al., 2016; Wang et al., 2016). Recordings from each epicortical electrode during the poststimulus period are compared to the prestimulus baseline on an epoch-by-epoch basis on gamma power. A statistical criterion is then applied to determine time windows during which gamma power is significantly elevated as compared to the baseline. The sites that correspond to the maximum significant elevations in gamma power are considered to be critically engaged in the task in question. This invasive method has adequate temporal resolution to discriminate between activity associated

THE AUDITORY AND ASSOCIATION CORTEX

469

Fig. 31.2. Placement of a 40-electrode grid on the left temporoparietal region during awake craniotomy in a patient undergoing surgery for intractable epilepsy. Stimulation by pairs of electrodes enclosed in the rectangle marked “R” during listening to short sentences produced difficulty in the immediate repetition of these sentences (i.e., stimulation of electrodes 36–37 produced a similar effect on repetition capacity as stimulation of electrodes 29–30). Stimulation of electrodes 29–30 resulted also in inability to name pictures of common objects. The rectangle marked “N” indicates the region where CSM produced naming deficits. The approximate location of the grid on the cortical surface is shown in the inset.

with stimulus processing and activity related to the preparation and execution of a spoken response to the stimulus. While considered as complementary to CSM for preoperative language mapping with satisfactory results (Babajani-Feremi et al., 2016; Wang et al., 2016; Arya et al., 2017), high gamma ECoG recordings can be used in the context of various paradigms to explore functional interactions within the circuits that support language (e.g., Brumberg et al., 2016; Rolston and Chang, 2017).

A SUMMARY OF THE SHORTCOMINGS OF THE INVASIVE PROCEDURES The most conspicuous shortcoming of the invasive procedures is the fact that they are associated with

appreciable morbidity. For the Wada procedure, the morbidity levels vary between 3% and 5% (Dion et al., 1987; Young et al., 2002). The rates of infection associated with subdural grid electrodes for the dual purpose of localization of the ictal onset zone and extraoperative CSM range from 1.5% to 12.1% (Wiggins et al., 1999; Hamer et al., 2002; Van Gompel et al., 2008). A second shortcoming of the invasive procedures is patient discomfort; a third is the inability to identify memory-specific circuitry via CSM and the questionable efficiency of the Wada procedure in identifying the memory-dominant hemisphere. Thus, the neuronal circuitry responsible for the formation of memories is inaccessible to CSM, and no improvement of the procedure is possible in that respect unless the limbic brain were to be probed by

470

A.C. PAPANICOLAOU ET AL.

depth electrodes. Equally uncertain may be the results of the Wada procedure for assessing memory. The uncertainty here derives from two sources: first from the fact that delivery of the sodium amobarbital to the hippocampal formation is not always possible (Jeffery et al., 1991; McMackin et al., 1997)—a limitation of the procedure that cannot be overcome; and second, from the fact that the way the Wada protocol is structured does not allow for separate estimation of hemispheric dominance for verbal and nonverbal encoding. Moreover, although it is true that separate evaluation for verbal and nonverbal memory is conceivable with a modification of the commonly used Wada protocol described earlier, it would increase the examination time, which is another problem common to the invasive procedures. The fourth and fifth limitations of CSM and the Wada are intimately related to the narrow time window in which they have to be performed: repetition of the procedures for the purpose of establishing reliability of the results is nearly impossible in the case of Wada and is very restricted in the case of CSM. Moreover, neither CSM nor the Wada probes for the mechanisms of a host of different cognitive operations that are subsumed under “language” and “memory” since they both involve very simple and coarse tasks. For example, object naming, sentence comprehension, and various other tasks that involve language and memory may share a number of local networks that can be disrupted by CSM, but they also require others, specific to each, that cannot be identified through CSM precisely because of time limitations. A sixth limitation specific to CSM is the inability to precisely control the spread of the current and the inability to control for cross flow, specific to the Wada procedure, rendering uncertain the degree of functional suppression of the hemisphere injected (McMackin et al., 1997). A seventh problem, in part reducible to the time constraints as the previous two, is the inability to control for situational variables that may corrupt the integrity of the data. Lapses in attention on the part of the patient in the crowded suite where a number of tasks have to be done under time constraints may well produce misleading data, the integrity of which is impossible to ascertain since the procedure is done only once. In the case of CSM, situational variability is mostly contributed by the following factors: (1) sedation level, not always optimal for keeping the patient comfortable and at the same time sufficiently alert to complete the procedure; (2) current leakage along the cortical surface, the extent of which depends on the degree of tissue hydration; and (3) the timing of the delivery of CSM with respect to the task, which usually varies from trial to trial given that, in most cases, task-specific stimuli

and the stimulating current are delivered manually and not through a computer. In spite of these shortcomings, these two invasive procedures are still considered to be the gold standards, although noninvasive language evaluation alternatives are slowly gaining ascendancy and in several centers are used to supplement and in certain occasions to replace the invasive ones, especially in those cases where application of the invasive methods is, for any of a number of reasons, impractical or impossible. Recently, the use of one of the noninvasive methods, briefly reviewed in the next section, was endorsed by a panel of the American Academy of Neurology as a substitute for the Wada procedure in temporal lobe epilepsy cases for assessing hemispheric dominance for language (Szaflarski et al., 2017).

NONINVASIVE LANGUAGE EVALUATION PROCEDURES Three noninvasive procedures are typically used for assessment of hemispheric dominance for language, as well as for localization of cortical patches within the dominant hemisphere: transcranial magnetic stimulation (TMS), which is used as a functional equivalent of CSM in the sense that it too produces reversible lesions; magnetoencephalography (MEG); and functional magnetic resonance imaging (fMRI).

TMS This procedure is based on the fact that a current passing through a coil results in a magnetic field that passes through the scalp and skull and induces current in the underlying brain tissue. The neurons in the path of this current depolarize and fire synchronously. This has either an excitatory or an inhibitory effect depending on the location and parameters of stimulation. The former is used in mapping the motor cortex and the latter for localizing the language-specific cortex using trains of stimulating pulses (e.g., Pascual-Leone et al., 1991). The most common task used in language mapping with TMS is object naming. First, baseline performance during the task is recorded. Next, repetitive TMS is delivered to presumed language-related areas in both hemispheres as the patients perform the task. Usually, picture stimuli are presented for 500–2000 ms (based on the patient’s ability) with interstimulus intervals of 4–5 s. The onset of TMS is time-locked to either the time of stimulus onset or 200–300 ms following the stimulus onset. TMS is typically applied at a rate of 10 or 5 Hz for 500–1000 ms duration (five pulses total). The patient’s responses during TMS are videorecorded and analyzed after the session for errors and speech disruption. The brain areas where TMS

THE AUDITORY AND ASSOCIATION CORTEX

471

Fig. 31.3. (Upper panel) Set-up of TMS study. The coil emitting magnetic pulses is placed using a stereotactic system enabling precise localization of the affected cortical regions on the person’s MRI. (Lower panel) Stimulated sites aggregated over a group of nine patients who also underwent CSM. Black and blue circles indicate locations of positive magnetic stimulation effects (i.e., producing some form of speech disruption). Only a small portion of this region was found to be essential for speech production based on CSM results (shaded gray area).

stimulation results in speech arrest, performance errors, and semantic errors are identified on the patient’s MRI (see Fig. 31.3).

MEG A second noninvasive method for somatosensory motor and language mapping is MEG. For receptive language

mapping with MEG, variations of the following task (Castillo et al., 2001; Papanicolaou et al., 2004) may be used: patients are given a recognition memory task for spoken words, and event-related fields are recorded for each word stimulus. The stimuli (target words that are repeated and foils that are presented once) are delivered binaurally with an intensity of 80 dB sound pressure level at the patient’s outer ear through two plastic tubes

472

A.C. PAPANICOLAOU ET AL.

Fig. 31.4. (Left-hand panel) Averaged MEG waveforms in response to a series of spoken words presented in the context of a continuous word recognition task in the context of preoperative mapping in a patient suffering from a left temporoparietal tumor. Onset of stimuli is at 0 ms. As is customary, recordings were obtained during two repetitions of the same task (using a different set of words each time). The bracket indicates the time window considered for the localization of cortical sources of magnetic activity associated with word recognition and discrimination of “old” (i.e., trained) vs “new” (i.e., untrained) words. (Right-hand panel) Locations of dipolar sources in the left posterior temporal lobe estimated at successive time points during the analysis window. Active regions that are more likely to reflect linguistic processing are estimated through a two-step process. First, temporal filtering is applied by excluding cortical sources in primary auditory cortices. Second, spatial filtering is performed by identifying regions that consistently display activity sources across the two repetitions of the activation task.

terminating in ear inserts with a variable interstimulus interval of 2.5–3.5 s. Patients are asked to lift their index finger whenever they recognize a repeated word. The responding hand is counterbalanced across sessions (see Fig. 31.4). On occasion, a variation of this protocol has been adopted in the visual modality, whereby target and distractor stimuli are presented visually, with identical task demands (e.g., Breier et al., 2001). As well as eliciting reliable receptive language cortex activation, the visual variant of the task has been shown to engage the inferior frontal region (see Papanicolaou et al., 2006). Although MEG receptive language mapping has most readily been achieved using the aforementioned protocol, adoption of other paradigms (e.g., Bowyer et al., 2005; Kamada et al., 2007) has been shown to be equally useful in identifying receptive language cortex. Expressive language mapping using MEG is typically performed in the context of a picture naming task (e.g., Castillo et al., 2001; Bowyer et al., 2004) or a covert verb generation task (e.g., Bowyer et al., 2005; Findlay et al., 2012).

fMRI The most common task for expressive language mapping with fMRI involves covert production of words to visual cues. Several variants of this task are in use. In verb generation tasks, the patient is asked to silently produce action verbs (e.g., “cut, slice”) in response to a printed noun (e.g., “knife”). Another common variant of word

generation tasks involves the production of nouns that belong to a semantic category label presented either visually or auditorily to the patient during the active blocks. Activation maps obtained during these tasks are compared to activation maps obtained during rest or during passing viewing of meaningless letter strings. Alternative tasks often used for expressive language mapping involve covert object naming and sentence completion. A typical object naming task consists of a standard block design alternating between stimulus and rest, during which the patient is presented with line drawings of living and inanimate objects (Szekely et al., 2005), with the explicit instruction to covertly name the object upon presentation. The sentence completion task may follow that described, for example, by Ashtari et al. (2005), whereby, during the activation blocks, the patient is visually presented with a display of simple sentences with a blank space at the end and is required to complete the sentence on the basis of its meaning (see Fig. 31.5). Receptive language mapping with fMRI generally follows the protocol described by Binder et al. (1995) involving a blocked semantic/tone decision task (see also Janecek et al., 2013). In summary, patients are presented with names of animals and cued to make a button response regarding a particular attribute of the animal. This condition is alternated with a tone decision task where patients are presented with sequences of highand low-frequency tones and instructed to make a button response upon hearing a sequence containing two high tones. Indeed, fMRI has been used to reduce the extent

THE AUDITORY AND ASSOCIATION CORTEX

0

24

Sentence

48

Nonsense text

72

Sentence

473

96 s

Nonsense text

Fig. 31.5. (Left-hand panel) A typical fMRI paradigm designed to elicit activation associated with both (covert) expressive and receptive language functions (sentence completion task). Series of four printed sentences are presented for 24 s followed by series of nonsense sentence-like text (also for 24 s). A blood oxygen level-dependent signal is recorded in the form of a continuous time series from each image element of the brain (voxel). Recordings from brain regions that display increased activation during the sentence blocks in relation to the nonsense blocks are expected to display regular systematic fluctuations such as those exhibited by the waveform (blue line). Activation maps consist of voxels where BOLD signal during the sentence blocks is significantly higher than BOLD signal during nonsense blocks at a predetermined statistical criterion (here at t > 4.0). (Right-hand panel) Activation maps from a single participant that meet an additional criterion: spatial overlap across two repetitions of the task, featuring active voxels in inferior frontal and posterior temporal regions. Adapted from Voyvodic JT (2012). Reproducibility of single-subject fMRI language mapping with AMPLE normalization. J Magn Reson Imaging 36: 69–80.

of the cortical surface explored through CSM and therefore decrease the duration of the surgical procedure on the strength of the assumption that fMRI provides the requisite sensitivity for detecting the relevant cortex and CSM provides the requisite specificity (Pillai et al., 2010). However, no reports have shown a clear difference in surgical approach or outcomes by adding CSM to the fMRI.

THE COMPATIBILITY OF THE INVASIVE AND NONINVASIVE METHODS The compatibility of the language lateralization results of the Wada and fMRI procedures has been attested to in a number of studies with patient samples ranging from 7 to 100 individuals. Results range from reporting perfect concordance (Desmond et al., 1995; Benson et al., 1999; Deblaere et al., 2004) to nearly perfect (Binder et al., 1996; Hertz-Pannier et al., 1997; Carpentier et al., 2001; Sabbah et al., 2003; Woermann et al., 2003) or considerably high (Lehericy et al., 2000; Benke et al., 2006; Szaflarski et al., 2008; Arora et al., 2009; Suarez et al., 2009; Jones et al., 2011; Zaca et al., 2012; Janecek et al., 2013). Also high is the reported compatibility between the results of the Wada and MEG with respect to language lateralization, reaching 87% concordance in the study with the largest sample (Papanicolaou et al., 2004), with the rest of the studies reporting uniformly high agreement (Breier et al., 2001; Maestu et al., 2002; Hirata et al., 2004, 2010; Bowyer et al., 2005; Merrifield et al.,

2007; Doss et al., 2009; McDonald et al., 2009; Findlay et al., 2012; Tanaka et al., 2013). Far fewer studies report comparisons of laterality estimates for memory between fMRI and Wada. These involve small samples yet high concordance (Detre et al., 1998; Golby et al., 2002) but also low (Deblaere et al., 2005), and none are between MEG and Wada. Furthermore, quite high is the degree of concordance between CSM and MEG localization of languagespecific cortical patches. In a study involving a small patient sample, Simos et al. (1999) showed compatibility of CSM and MEG for localizing receptive languagespecific cortical sites, as did a second study involving 47 patients (Castillo and Papanicolaou, 2005). The same is the case with TMS: in a recent study, Picht et al. (2013) performed presurgical language mapping with navigated TMS in 20 patients with tumors in the perisylvian region using a picture naming task. Compared to CSM findings, the sensitivity of TMS was very high in identifying language-related patches across posterior and anterior regions (90.2%) and in identifying expressive language-related cortex (100%). Results, however, revealed rather poor specificity of TMS (23.8% and 13.0%, respectively) associated with a high rate of false-positive TMS results, especially when applied to inferior frontal regions. Thus, noninvasive language mapping with TMS is emerging as a valuable tool for preoperative mapping of language areas. Moreover, Tarapore et al. (2012) demonstrated that the maps of the motor system generated with TMS correlate well with those generated by both MEG and CSM and that

474

A.C. PAPANICOLAOU ET AL.

negative TMS mapping also correlates with negative CSM mapping. Furthermore, the motor maps generated by TMS have been shown to be spatially consistent across multiple sessions (McGregor et al., 2012). The question then arises as to interpretation of discordant localization and lateralization results between the invasive and noninvasive methods. On the basis of the assumption that CSM and the Wada test are the gold standards, the tendency is to consider discordant estimates as failures of the noninvasive methods. However, when that assumption was put to empirical test, it became obvious that neither CSM results nor those of the Wada should be considered as the gold standard any more than the results of the noninvasive methods should. For example, using CSM, Ojemann (1990, 1991) reported extensive temporal lobe involvement in receptive language tasks such as naming, yet Sanai et al. (2008), also using CSM, found a paucity of naming sites there. Besides limited reliability, CSM also has limited predictive value with respect to postsurgical language and memory performance when the latter is also operationally defined as performance in naming tasks. For example, Ojemann and Dodrill (1985) reported 80% predictive accuracy of CSM. Cervenka et al. (2013) reported that in a series of 7 patients, language deficits were not anticipated by CSM data, because four had amygdalohippocampectomies and, more importantly, because three developed language deficits, although CSM-determined languagespecific loci were not resected. Cervenka et al. (2011) reported that three of four patients operated presented language deficits that were not predicted by CSM; Hamberger et al. (2005) reported that in their experience sparing cortical sites that were CSM positive (i.e., their stimulation interrupted naming) did not prevent postoperative word finding difficulties; Hermann et al. (1999) in their review of the results of 8 centers involving 217 patients concluded that neither intra- nor extraoperative CSM-guided surgeries are any more effective in reducing postoperative naming deficits than non-CSM-guided surgeries. The efficacy of the Wada procedure is also lower than would be expected for a gold standard for predicting the likelihood of postoperative language and memory deficits. In fact, the assertion that it is correctly assessing language laterality was not empirically verified against surgical outcome until recently, in the context of comparing its efficacy against that of fMRI. Such comparisons show that fMRI may have better predictive efficacy than the Wada test (Sabsevitz et al., 2003). Equally limited is the efficacy of the Wada procedure in predicting memory outcome. Prediction of verbal memory performance postoperatively varies from good (Kneebone et al., 1995; Loring et al., 1995; Bell et al., 2000; Chiaravalloti and Glosser, 2001; Sabsevitz et al.,

2001) to very low (Chelune et al., 1991; Stroup et al., 2003; Lacruz et al., 2004; Kirsch et al., 2005; Lineweaver et al., 2006; Binder et al., 2008). Meanwhile, dozens of studies are conducted every year for the purpose of fine-tuning the noninvasive methods, to reveal with increasing reliability brain regions involved in different aspects of memory and language performance using fMRI (e.g., Jansen et al., 2009; Seghier et al., 2011; Strandberg et al., 2011; Niskanen et al., 2012), MEG (e.g., Papanicolaou et al., 2002, 2006; Kim and Chung, 2008; Mohamed et al., 2008; Riggs et al., 2009; Passaro et al., 2013) and TMS (Coburger et al., 2012; Tarapore et al., 2012; Picht et al., 2013), and verifying the validity of the findings, mainly against prior knowledge gained by the long experience of lesion studies. For nearly 2 decades MEG, fMRI, and TMS data have been used as adjunct means of assessing language and memory laterality and language localization. In some cases, MEG especially has been used as a means of informing the placement of subdural grid electrodes (Blount et al., 2008; Ochi and Otsubo, 2008; Vitikainen et al., 2009) in the process of identifying the location and extent of the epileptogenic zones. The question though remains: can the noninvasive procedures used in tandem replace CSM and the Wada test? This issue is currently debated (see, e.g., Papanicolaou et al., 2014) and until resolved the invasive procedures will remain in many, but not necessarily in most, clinicians’ minds the gold standards for the presurgical evaluation of language.

REFERENCES Arora J, Pugh K, Westerveld M et al. (2009). Language lateralization in epilepsy patients: fMRI validated with the Wada procedure. Epilepsia 50: 2225–2241. Arya R, Wilson JA, Fujiwara H et al. (2017). Presurgical language localization with visual naming associated ECoG high-gamma modulation in pediatric drug-resistant epilepsy. Epilepsia 58: 663–673. Ashtari M, Perrine K, Elbaz R et al. (2005). Mapping the functional anatomy of sentence comprehension and application to presurgical evaluation of patients with brain tumor. Am J Neuroradiol 26: 1461–1468. Babajani-Feremi A, Narayana S, Rezaie R et al. (2016). Language mapping using high gamma electrocorticography, fMRI, and TMS versus electrocortical stimulation. Clin Neurophysiol 127: 1822–1836. Baldo JV, Klostermann EC, Dronkers NF (2008). It’s either a cook or a baker: patients with conduction aphasia get the gist but lose the trace. Brain Lang 105: 134–140. Bell BD, Davies KG, Hermann BP et al. (2000). Confrontation naming after anterior temporal lobectomy is related to age of acquisition of the object names. Neuropsychologia 38: 83–92.

THE AUDITORY AND ASSOCIATION CORTEX Benke T, Koylu B, Visani P et al. (2006). Language lateralization in temporal lobe epilepsy: a comparison between fMRI and the Wada test. Epilepsia 47: 1308–1319. Benson RR, FitzGerald DB, LeSueur LL et al. (1999). Language dominance determined by whole brain functional MRI in patients with brain lesions. Neurology 52: 798–809. Binder JR, Rao SM, Hammeke TA et al. (1995). Lateralized human brain language systems demonstrated by task subtraction functional magnetic resonance imaging. Arch Neurol 52: 593–601. Binder JR, Swanson SJ, Hammeke TA et al. (1996). Determination of language dominance using functional MRI: a comparison with the Wada test. Neurology 46: 978–984. Binder JR, Sabsevitz DS, Swanson SJ et al. (2008). Use of preoperative functional MRI to predict verbal memory decline after temporal lobe epilepsy surgery. Epilepsia 49: 1377–1394. Blount JP, Cormier J, Kim H et al. (2008). Advances in intracranial monitoring. Neurosurg Focus 25: E18. Bogen JE, Bogen GM (1976). Wernicke’s region—Where is it? Ann N Y Acad Sci 280: 834–843. Bowyer SM, Moran JE, Mason KM et al. (2004). MEG localization of language-specific cortex utilizing MR-FOCUSS. Neurology 62: 2247–2255. Bowyer SM, Moran JE, Weiland BJ et al. (2005). Language laterality determined by MEG mapping with MR-FOCUSS. Epilepsy Behav 6: 235–241. Breier JI, Simos PG, Wheless JW et al. (2001). Language dominance in children as determined by magnetic source imaging and the intracarotid amobarbital procedure: a comparison. J Child Neurol 16: 124–130. Brumberg JS, Krusienski DJ, Chakrabarti S et al. (2016). Spatio-temporal progression of cortical activity related to continuous overt and covert speech production in a reading task. PLoS One 11 (11): e0166872. Buchman AS, Garron DC, Trost-Cardamone JE et al. (1986). Word deafness: one hundred years later. J Neurol Neurosurg Psychiatry 49: 489–499. Buchsbaum B, Pickell B, Love T et al. (2005). Neural substrates for verbal working memory in deaf signers: fMRI study and lesion case report. Brain Lang 95: 265–272. Buchsbaum BR, Baldo J, Okada K et al. (2011). Conduction aphasia, sensory-motor integration, and phonological short-term memory—an aggregate analysis of lesion and fMRI data. Brain Lang 119: 119–128. Carpentier A, Pugh KR, Westerveld M et al. (2001). Functional MRI of language processing: dependence on input modality and temporal lobe epilepsy. Epilepsia 42: 1241–1254. Castillo EM, Papanicolaou AC (2005). Cortical representation of dermatomes: MEG-derived maps after tactile stimulation. Neuroimage 25: 727–733. Castillo EM, Simos PG, Venkataraman V et al. (2001). Mapping of expressive language cortex using magnetic source imaging. Neurocase 7: 419–422. Cervenka MC, Boatman-Reich DF, Ward J et al. (2011). Language mapping in multilingual patients: electrocorticography and cortical stimulation during naming. Front Hum Neurosci 5: 13.

475

Cervenka MC, Corines J, Boatman-Reich DF et al. (2013). Electrocorticographic functional mapping identifies human cortex critical for auditory and visual naming. Neuroimage 69: 267–276. Chelune GJ, Naugle RI, Luders H et al. (1991). Prediction of cognitive change as a function of preoperative ability status among temporal lobectomy patients seen at 6-month follow-up. Neurology 41: 399–404. Chiaravalloti ND, Glosser G (2001). Material-specific memory changes after anterior temporal lobectomy as predicted by the intracarotid amobarbital test. Epilepsia 42: 902–911. Coburger J, Karhu J, Bittl M et al. (2012). First preoperative functional mapping via navigated transcranial magnetic stimulation in a 3-year-old boy. J Neurosurg Pediatr 9: 660–664. Damasio H, Damasion AR (1980). The anatomical basis of conduction aphasia. Brain 103: 337–350. Deblaere K, Boon PA, Vandemaele P et al. (2004). MRI language dominance assessment in epilepsy patients at 1.0 T: region of interest analysis and comparison with intracarotid amytal testing. Neuroradiology 46: 413–420. Deblaere K, Backes WH, Tieleman A et al. (2005). Lateralized anterior mesiotemporal lobe activation: semirandom functional MR imaging encoding paradigm in patients with temporal lobe epilepsy—initial experience. Radiology 236: 996–1003. Desmond JE, Sum JM, Wagner AD et al. (1995). Functional MRI measurement of language lateralization in Wadatested patients. Brain 118 (Pt 6): 1411–1419. Detre JA, Maccotta L, King D et al. (1998). Functional MRI lateralization of memory in temporal lobe epilepsy. Neurology 50: 926–932. Dion JE, Gates PC, Fox AJ et al. (1987). Clinical events following neuroangiography: a prospective study. Stroke 18: 997–1004. Doss RC, Zhang W, Risse GL et al. (2009). Lateralizing language with magnetic source imaging: validation based on the Wada test. Epilepsia 50: 2242–2248. Findlay AM, Ambrose JB, Cahn-Weiner DA et al. (2012). Dynamics of hemispheric dominance for language assessed by magnetoencephalographic imaging. Ann Neurol 71: 668–686. Geschwind N (1972). Language and the brain. Sci Am 226: 76–83. Golby AJ, Poldrack RA, Illes J et al. (2002). Memory lateralization in medial temporal lobe epilepsy assessed by functional MRI. Epilepsia 43: 855–863. Goodglass H (1993). Understanding aphasia, Academic Press, San Diego. Gorno-Tempini ML, Dronkers NF, Rankin KP et al. (2004). Cognition and anatomy in three variants of primary progressive aphasia. Ann Neurol 55: 335–346. Hamberger MJ, Seidel WT, McKhann 2nd GM et al. (2005). Brain stimulation reveals critical auditory naming cortex. Brain 128: 2742–2749. Hamer HM, Morris HH, Mascha EJ et al. (2002). Complications of invasive video-EEG monitoring with subdural grid electrodes. Neurology 58: 97–103.

476

A.C. PAPANICOLAOU ET AL.

Hermann B, Davies K, Foley K et al. (1999). Visual confrontation naming outcome after standard left anterior temporal lobectomy with sparing versus resection of the superior temporal gyrus: a randomized prospective clinical trial. Epilepsia 40: 1070–1076. Hertz-Pannier L, Gaillard WD, Mott SH et al. (1997). Noninvasive assessment of language dominance in children and adolescents with functional MRI: a preliminary study. Neurology 48: 1003–1012. Hickok G, Poeppel D (2000). Towards a functional neuroanatomy of speech perception. Trends Cogn Sci 4: 131–138. Hickok G, Poeppel D (2007). The cortical organization of speech processing. Nat Rev Neurosci 8: 393–402. Hickok G, Poeppel D (2015). Neural basis of speech perception. In: MJ Aminoff, F Boller, DF Swaab (Eds.), Handbook of clinical neurology, third edn. Elsevier 149–160. Hickok G, Buchsbaum B, Humphries C et al. (2003). Auditorymotor interaction revealed by fMRI: speech, music, and working memory in area Spt. J Cogn Neurosci 15: 673–682. Hirata M, Kato A, Taniguchi M et al. (2004). Determination of language dominance with synthetic aperture magnetometry: comparison with the Wada test. Neuroimage 23: 46–53. Hirata M, Goto T, Barnes G et al. (2010). Language dominance and mapping based on neuromagnetic oscillatory changes: comparison with invasive procedures. J Neurosurg 112: 528–538. Hodges JR, Patterson K, Oxbury S et al. (1992). Semantic dementia. Progressive fluent aphasia with temporal lobe atrophy. Brain 115 (Pt 6): 1783–1806. Hurley RS, Paller KA, Rogalski EJ et al. (2012). Neural mechanisms of object naming and word comprehension in primary progressive aphasia. J Neurosci 32: 4848–4855. Janecek JK, Swanson SJ, Sabsevitz DS et al. (2013). Language lateralization by fMRI and Wada testing in 229 patients with epilepsy: rates and predictors of discordance. Epilepsia 54: 314–322. Jansen A, Sehlmeyer C, Pfleiderer B et al. (2009). Assessment of verbal memory by fMRI: lateralization and functional neuroanatomy. Clin Neurol Neurosurg 111: 57–62. Jefferies E, Lambon Ralph MA (2006). Semantic impairment in stroke aphasia versus semantic dementia: a case-series comparison. Brain 129: 2132–2147. Jeffery PJ, Monsein LH, Szabo Z et al. (1991). Mapping the distribution of amobarbital sodium in the intracarotid Wada test by use of Tc-99m HMPAO with SPECT. Radiology 178: 847–850. Jones SE, Mahmoud SY, Phillips MD (2011). A practical clinical method to quantify language lateralization in fMRI using whole-brain analysis. Neuroimage 54: 2937–2949. Kamada K, Sawamura Y, Takeuchi F et al. (2007). Expressive and receptive language areas determined by a non-invasive reliable method using functional magnetic resonance imaging and magnetoencephalography. Neurosurgery 60: 296–305. discussion 305-6. Kim JS, Chung CK (2008). Language lateralization using MEG beta frequency desynchronization during auditory oddball stimulation with one-syllable words. Neuroimage 42: 1499–1507.

Kirsch HE, Walker JA, Winstanley FS et al. (2005). Limitations of Wada memory asymmetry as a predictor of outcomes after temporal lobectomy. Neurology 65: 676–680. Kneebone AC, Chelune GJ, Dinner DS et al. (1995). Intracarotid amobarbital procedure as a predictor of material-specific memory change after anterior temporal lobectomy. Epilepsia 36: 857–865. Lacruz ME, Alarcon G, Akanuma N et al. (2004). Neuropsychological effects associated with temporal lobectomy and amygdalohippocampectomy depending on Wada test failure. J Neurol Neurosurg Psychiatry 75: 600–607. Lehericy S, Cohen L, Bazin B et al. (2000). Functional MR evaluation of temporal and frontal language dominance compared with the Wada test. Neurology 54: 1625–1633. Lhermitte F, Gautier JC (1969). Aphasia. In: P Vinken, G Bruyn (Eds.), Handbook of clinical neurology. NorthHolland Publishing Company, Amsterdam, pp. 84–104. Lineweaver TT, Morris HH, Naugle RI et al. (2006). Evaluating the contributions of state-of-the-art assessment techniques to predicting memory outcome after unilateral anterior temporal lobectomy. Epilepsia 47: 1895–1903. Loring DW, Lee GP, Meador KJ et al. (1990). The intracarotid amobarbital procedure as a predictor of memory failure following unilateral temporal lobectomy. Neurology 40: 605–610. Loring DW, Meador KJ, Lee GP et al. (1995). Wada memory asymmetries predict verbal memory decline after anterior temporal lobectomy. Neurology 45: 1329–1333. Luders H, Dinner DS, Lesser RP et al. (1986). Evoked potentials in cortical localization. J Clin Neurophysiol 3: 75–84. Luria AR (1970). Traumatic aphasia, Mouton, The Hague. Maestu F, Ortiz T, Fernandez A et al. (2002). Spanish language mapping using MEG: a validation study. Neuroimage 17: 1579–1586. Marie P (1906). The third left frontal convolution plays no special role in the function of language. Sem Med 26: 241–247. McDonald CR, Thesen T, Hagler Jr DJ et al. (2009). Distributed source modeling of language with magnetoencephalography: application to patients with intractable epilepsy. Epilepsia 50: 2256–2266. McGregor KM, Carpenter H, Kleim E et al. (2012). Motor map reliability and aging: a TMS/fMRI study. Exp Brain Res 219: 97–106. McMackin D, Dubeau F, Jones-Gotman M et al. (1997). Assessment of the functional effect of the intracarotid sodium amobarbital procedure using co-registered MRI/ HMPAO-SPECT and SEEG. Brain Cogn 33: 50–70. Merrifield WS, Simos PG, Papanicolaou AC et al. (2007). Hemispheric language dominance in magnetoencephalography: sensitivity, specificity, and data reduction techniques. Epilepsy Behav 10: 120–128. Mesulam MM, Wieneke C, Hurley R et al. (2013). Words and objects at the tip of the left temporal lobe in primary progressive aphasia. Brain 136: 601–618.

THE AUDITORY AND ASSOCIATION CORTEX Mesulam MM, Thompson CK, Weintraub S et al. (2015). The Wernicke conundrum and the anatomy of language comprehension in primary progressive aphasia. Brain 138: 2423–2437. Miceli G, Gainotti G, Caltagirone C et al. (1980). Some aspects of phonological impairment in aphasia. Brain Lang 11: 159–169. Mohamed IS, Cheyne D, Gaetz WC et al. (2008). Spatiotemporal patterns of oscillatory brain activity during auditory word recognition in children: a synthetic aperture magnetometry study. Int J Psychophysiol 68: 141–148. Naeser MA, Helm-Estabrooks N, Haas G et al. (1987). Relationship between lesion extent in ‘Wernicke’s area’ on computed tomographic scan and predicting recovery of comprehension in Wernicke’s aphasia. Arch Neurol 44: 73–82. Narain C, Scott SK, Wise RJ et al. (2003). Defining a left-lateralized response specific to intelligible speech using fMRI. Cereb Cortex 13: 1362–1368. Niskanen E, Kononen M, Villberg V et al. (2012). The effect of fMRI task combinations on determining the hemispheric dominance of language functions. Neuroradiology 54: 393–405. Ochi A, Otsubo H (2008). Magnetoencephalography-guided epilepsy surgery for children with intractable focal epilepsy: sickKids experience. Int J Psychophysiol 68: 104–110. Ojemann GA (1990). Organization of language cortex derived from investigations during neurosurgery. Semin Neurosci 2: 297–306. Ojemann GA (1991). Cortical organization of language. J Neurosci 11: 2281–2287. Ojemann GA, Dodrill CB (1985). Verbal memory deficits after left temporal lobectomy for epilepsy. Mechanism and intraoperative prediction. J Neurosurg 62: 101–107. Papanicolaou AC, Simos PG, Castillo EM et al. (2002). The hippocampus and memory of verbal and pictorial material. Learn Mem 9: 99–104. Papanicolaou AC, Simos PG, Castillo EM et al. (2004). Magnetocephalography: a noninvasive alternative to the Wada procedure. J Neurosurg 100: 867–876. Papanicolaou AC, Pazo-Alvarez P, Castillo EM et al. (2006). Functional neuroimaging with MEG: normative language profiles. Neuroimage 33: 326–342. Papanicolaou AC, Rezaie R, Narayana S et al. (2014). Is it time to replace the Wada test and put awake craniotomy to sleep? Epilepsia 55: 629–632. Pascual-Leone A, Gates JR, Dhuna A (1991). Induction of speech arrest and counting errors with rapid-rate transcranial magnetic stimulation. Neurology 41: 697–702. Passaro AD, Elmore LC, Ellmore TM et al. (2013). Explorations of object and location memory using fMRI. Front Behav Neurosci 7: 105. Patterson K, Nestor PJ, Rogers TT (2007). Where do you know what you know? The representation of semantic knowledge in the human brain. Nat Rev Neurosci 8: 976–987. Picht T, Krieg SM, Sollmann N et al. (2013). A comparison of language mapping by preoperative navigated transcranial magnetic stimulation and direct cortical stimulation during awake surgery. Neurosurgery 72: 808–819.

477

Pillai JJ, Zaca D, Choudhri AF (2010). Clinical impact of integrated physiologic brain tumor imaging. Technol Cancer Res Treat 9: 359–380. Price CJ (2012). A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading. Neuroimage 62: 816–847. Pulvermuller F (2013). How neurons make meaning: brain mechanisms for embodied and abstract-symbolic semantics. Trends Cogn Sci 17: 458–470. Pulvermuller F, Fadiga L (2010). Active perception: sensorimotor circuits as a cortical basis for language. Nat Rev Neurosci 11: 351–360. Rauschecker JP, Scott SK (2009). Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat Neurosci 12: 718–724. Riggs L, Moses SN, Bardouille T et al. (2009). A complementary analytic approach to examining medial temporal lobe sources using magnetoencephalography. Neuroimage 45: 627–642. Rogalsky C, Hickok G (2011). The role of Broca’s area in sentence comprehension. J Cogn Neurosci 23: 1664–1680. Rogalsky C, Pitz E, Hillis AE et al. (2008). Auditory word comprehension impairment in acute stroke: relative contribution of phonemic versus semantic factors. Brain Lang 107: 167–169. Rogers TT, Lambon Ralph MA, Garrard P et al. (2004). Structure and deterioration of semantic memory: a neuropsychological and computational investigation. Psychol Rev 111: 205–235. Rolston JD, Chang EF (2017). Critical language areas show increased functional connectivity in human cortex. Cereb Cortex17: 1–8. https://doi.org/10.1093/cercor/bhx271. Sabbah P, Chassoux F, Leveque C et al. (2003). Functional MR imaging in assessment of language dominance in epileptic patients. Neuroimage 18: 460–467. Sabsevitz DS, Swanson SJ, Morris GL et al. (2001). Memory outcome after left anterior temporal lobectomy in patients with expected and reversed Wada memory asymmetry scores. Epilepsia 42: 1408–1415. Sabsevitz DS, Swanson SJ, Hammeke TA et al. (2003). Use of preoperative functional neuroimaging to predict language deficits from epilepsy surgery. Neurology 60: 1788–1792. Sanai N, Mirzadeh Z, Berger MS (2008). Functional outcome after language mapping for glioma resection. N Engl J Med 358: 18–27. Schirmer A, Fox PM, Grandjean D (2012). On the spatial organization of sound processing in the human temporal lobe: a meta-analysis. Neuroimage 63: 137–147. Schwartz MF, Kimberg DY, Walker GM et al. (2009). Anterior temporal involvement in semantic word retrieval: voxel-based lesion-symptom mapping evidence from aphasia. Brain 132: 3411–3427. Scott SK, Blank CC, Rosen S et al. (2000). Identification of a pathway for intelligible speech in the left temporal lobe. Brain 123 (Pt. 12): 2400–2406. Seghier ML, Kherif F, Josse G et al. (2011). Regional and hemispheric determinants of language laterality: implications for preoperative fMRI. Hum Brain Mapp 32: 1602–1614.

478

A.C. PAPANICOLAOU ET AL.

Simos PG, Papanicolaou AC, Breier JI et al. (1999). Localization of language-specific cortex by using magnetic source imaging and electrical stimulation mapping. J Neurosurg 91: 787–796. Snowden JS, Goulding PJ, Neary D (1989). Semantic dementia: a form of circumscribed atrophy. Behav Neurol 2: 167–182. Spitsyna G, Warren JE, Scott SK et al. (2006). Converging language streams in the human temporal lobe. J Neurosci 26: 7328–7336. Strandberg M, Elfgren C, Mannfolk P et al. (2011). fMRI memory assessment in healthy subjects: a new approach to view lateralization data at an individual level. Brain Imaging Behav 5: 1–11. Stroup E, Langfitt J, Berg M et al. (2003). Predicting verbal memory decline following anterior temporal lobectomy (ATL). Neurology 60: 1266–1273. Suarez RO, Whalen S, Nelson AP et al. (2009). Thresholdindependent functional MRI determination of language dominance: a validation study against clinical gold standards. Epilepsy Behav 16: 288–297. Szaflarski JP, Holland SK, Jacola LM et al. (2008). Comprehensive presurgical functional MRI language evaluation in adult patients with epilepsy. Epilepsy Behav 12: 74–83. Szaflarski JP, Gloss D, Binder JR et al. (2017). Practice guideline summary: use of fMRI in the presurgical evaluation of patients with epilepsy: report of the Guideline Development, Dissemination, and Implementation Subcommittee of the American Academy of Neurology. Neurology 88: 395–402. Szekely A, D’Amico S, Devescovi A et al. (2005). Timed action and object naming. Cortex 41: 7–25. Tanaka N, Liu H, Reinsberger C et al. (2013). Language lateralization represented by spatiotemporal mapping of magnetoencephalography. Am J Neuroradiol 34: 558–563. Tarapore PE, Tate MC, Findlay AM et al. (2012). Preoperative multimodal motor mapping: a comparison of magnetoencephalography imaging, navigated transcranial magnetic stimulation, and direct cortical stimulation. J Neurosurg 117: 354–362. Turkeltaub PE, Coslett HB (2010). Localization of sublexical speech perception components. Brain Lang 114: 1–15. Turken AU, Dronkers NF (2011). The neural architecture of the language comprehension network: converging evidence from lesion and connectivity analyses. Front Syst Neurosci 5: 1. Van Gompel JJ, Worrell GA, Bell ML et al. (2008). Intracranial electroencephalography with subdural grid electrodes: techniques, complications, and outcomes. Neurosurgery 63: 498–505. discussion 505-6. Vitikainen AM, Lioumis P, Paetau R et al. (2009). Combined use of non-invasive techniques for improved functional localization for a selected group of epilepsy surgery candidates. Neuroimage 45: 342–348. Wang Y, Fifer MS, Flinker A et al. (2016). Spatial-temporal functional mapping of language at the bedside with electrocorticography. Neurology 86: 1181–1189.

Wernicke C (1874/1969). The symptom complex of aphasia: a psychological study on an anatomical basis. In: RS Cohen, MW Wartofsky (Eds.), Boston studies in the philosophy of science. D. Reidel Publishing Company, Dordrecht, pp. 34–97. Wiggins GC, Elisevich K, Smith BJ (1999). Morbidity and infection in combined subdural grid and strip electrode investigation for intractable epilepsy. Epilepsy Res 37: 73–80. Woermann FG, Jokeit H, Luerding R et al. (2003). Language lateralization by Wada test and fMRI in 100 patients with epilepsy. Neurology 61: 699–701. Young N, Chi KK, Ajaka J et al. (2002). Complications with outpatient angiography and interventional procedures. Cardiovasc Intervent Radiol 25: 123–126. Zaca D, Nickerson JP, Deib G et al. (2012). Effectiveness of four different clinical fMRI paradigms for preoperative regional determination of language lateralization in patients with brain tumors. Neuroradiology 54: 1015–1025.

FURTHER READING Binder JR, Swanson SJ, Sabsevitz DS et al. (2010). A comparison of two fMRI methods for predicting verbal memory decline after left temporal lobectomy: language lateralization versus hippocampal activation asymmetry. Epilepsia 51: 618–626. Birg L, Narayana S, Rezaie R et al. (2013). Technical tips: MEG and EEG with sedation. Neurodiagn J 53: 229–240. Breier JI, Simos PG, Zouridakis G et al. (1999). Lateralization of cerebral activation in auditory verbal and non-verbal memory tasks using magnetoencephalography. Brain Topogr 12: 89–97. Castillo EM, Simos PG, Wheless JW et al. (2004). Integrating sensory and motor mapping in a comprehensive MEG protocol: clinical validity and replicability. Neuroimage 21: 973–983. Ganslandt O, Fahlbusch R, Nimsky C et al. (1999). Functional neuronavigation with magnetoencephalography: outcome in 50 patients with lesions around the motor cortex. J Neurosurg 91: 73–79. Krishnan R, Raabe A, Hattingen E et al. (2004). Functional magnetic resonance imaging-integrated neuronavigation: correlation between lesion-to-motor cortex distance and outcome. Neurosurgery 55: 904–914. discussion 914-5. Makela JP, Kirveskari E, Seppa M et al. (2001). Threedimensional integration of brain anatomy and function to facilitate intraoperative navigation around the sensorimotor strip. Hum Brain Mapp 12: 180–192. Pataraia E, Simos PG, Castillo EM et al. (2004). Reorganization of language-specific cortex in patients with lesions or mesial temporal epilepsy. Neurology 63: 1825–1832. Rao SM, Bandettini PA, Binder JR et al. (1996). Relationship between finger movement rate and functional magnetic resonance signal change in human primary motor cortex. J Cereb Blood Flow Metab 16: 1250–1254.

THE AUDITORY AND ASSOCIATION CORTEX Rossi S, Hallett M, Rossini PM et al. (2009). Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120: 2008–2039. Rossini PM, Barker AT, Berardelli A et al. (1994). Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 91: 79–92. Shriver S, Knierim KE, O’Shea JP et al. (2013). Pneumatically driven finger movement: a novel passive functional MR

479

imaging technique for presurgical motor and sensory mapping. Am J Neuroradiol 34: E5–E7. Shurtleff H, Warner M, Poliakov A et al. (2010). Functional magnetic resonance imaging for presurgical evaluation of very young pediatric patients with epilepsy. J Neurosurg Pediatr 5: 500–506. Wassermann EM, Zimmermann T (2012). Transcranial magnetic brain stimulation: therapeutic promises and scientific gaps. Pharmacol Ther 133: 98–107. Witt ST, Laird AR, Meyerand ME (2008). Functional neuroimaging correlates of finger-tapping task variations: an ALE meta-analysis. Neuroimage 42: 343–356.