Analysis of naming errors during cortical stimulation mapping: Implications for models of language representation
Introduction
Complementing the results of neuroimaging and lesion studies, cortical stimulation mapping (CSM) provides a rare and valuable opportunity for mapping language function to neuroanatomy (Ojemann, 1991). CSM is an invasive procedure used to identify the language, sensory, and motor cortices, so that these critical regions may be preserved during surgical resection. The technique was originally employed to identify the sensory-motor cortices in patients with medically intractable seizure disorders. Penfield and colleagues later extended the procedure to identify eloquent language cortex by implementing an object-naming task (Penfield & Roberts, 1959). Subsequent studies have demonstrated that visual naming under stimulation can successfully identify resection boundaries that preserve functionally important language areas (Haglund, Berger, Shamseldin, Lettich, & Ojemann, 1994; Ojemann, 1983), though some controversy remains (e.g., Seeck et al., 2006).
CSM is one of the few techniques that allow direct observation of language dysfunction at an extremely localized neural level. However, the technique is limited by its own unique constraints. As a surgical procedure, intraoperative mapping is limited in time, with most testing typically lasting 0.5–3 h (Gordon, Boatman, Hart, Miglioretti, & Lesser, 2001). Cortical stimulation sites are limited to the regions exposed by the craniotomy (Roux et al., 2004). Typically there is an unequal sampling of cortical sites within the exposed region. Moreover, patients have just come out of general anesthesia and may be lethargic and therefore not alert or in the most optimal state for testing (Gordon et al., 2001). In addition, neurologically compromised patients, especially those with an early-age epilepsy onset, may have undergone cortical reorganization (Thompson, 2005). Aside from these procedural constraints, some controversy remains over the extent to which electrical stimulation spreads to adjacent cortex (Ojemann, 1983). Some studies of non-human primates have reported greater than expected spread of current in visual cortex (Tolias et al., 2005), though other studies have reported a lack of activation in adjacent cortex (Haglund, Ojemann, & Blasdel, 1993).
Despite these challenges, cortical stimulation studies over the past three decades have provided valuable evidence of the cortical organization of language. Although lesion studies have identified classic perisylvian regions in language processing, CSM studies have shown that language cortex may involve extra-sylvian regions, though these are variable across patients. Although most language sites are distinctly defined by sharp boundaries, some regions have been reported to include a “fuzzy” transition zone where cortical stimulation induces only occasional naming disruption (Whitaker & Ojemann, 1977). CSM studies comparing early and adult lesion onset (Ojemann, Ojemann, Lettich, & Berger, 1989) and patients with fast growing tumors reveal a highly similar pattern of language organization, suggesting that this mosaic of language function spread across perisylvian regions is likely reflective of the general population and is not simply an artifact of language organization in a clinical epileptic population.
CSM studies have provided evidence that cortex can exhibit functionally specific vulnerabilities for language functions. Direct cortical stimulation has given rise to specific and differentiated errors associated with reading, verbal memory, semantic classes, and differential object naming in bilinguals (Ojemann, 2003). Evidence of selective disruption of verb versus noun naming has been reported (Corina et al., 2005), as well as dissociations of reading and object naming (Roux et al., 2004). An anterior to posterior distribution for auditory versus visual naming has also been reported (Hamberger, McClelland, McKhann, Williams, & Goodman, 2007). A number of CSM speech perception studies have identified discrete regions in the middle-posterior superior temporal gyrus that subserve phonological processing of consonants but not vowels (Boatman et al., 1997, Boatman et al., 1995).
In the present study, we add to this body of literature a characterization of the type and distribution of naming errors observed during CSM. Specifically, we examine the neuroanatomical correlates and linguistic characteristics of six common naming errors: semantic paraphasias, circumlocutions, phonological paraphasias, neologisms, performance errors, and no-response errors.
Section snippets
Patients
The present study queried a database of 110 patients (57 female, 53 male; age range 15–61) undergoing CSM as part of intractable epilepsy surgery or tumor resection at the University of Washington Medical Center. Patients were included in this study if: (a) they produced one or more stimulated errors of our five primary error types (i.e. semantic, phonological, neologism, circumlocution, or performance) and (b) imaging data was available to conduct site localization. This procedure identified
Error types
Regarding error type, the most frequently observed errors were no-response errors (54.0%), followed by performance errors (16.4%) and semantic paraphasias (15.1%). Less frequent errors included phonological paraphasias (7.4%), neologisms (4.0%), and circumlocutions (3.1%). Table 3 presents the raw error data by region and type for all cortical regions and it shows the number of patients observed to have made one or more target errors during electrocortical stimulation.
Semantic paraphasias
Semantic paraphasias were
Semantic paraphasias
Semantic paraphasias were one of the most prevalent naming errors observed. Examining the semantic relationship between target form and error, we found that patients made proportionally more coordinate-level errors (lion → ‘tiger’) than other errors. Regarding the distribution of semantic paraphasias, we observed wide spread regions in the temporal and parietal lobes giving rise to semantic paraphasias, the most prominent of which include mPoG, aSMG, and pMTG.
In most current models of language
Conclusion
In summary, several valuable confirmatory as well as novel findings emerge from this study. Current models of language processing acknowledge a wide distribution of cortical regions implicated in the language network. Our data demonstrate that errors in object naming may arise from widespread regions within perisylvian areas. However, our data also indicate that the network is functionally heterogeneous and honors distinctions between frontal, parietal, and posterior temporal dorsal
Acknowledgments
This work was supported in part by Grants National Institutes of Health [DC003099 to DC; DC02310 to JB and HL087706 to JB]. We thank Nina Dronkers for previous comments.
References (70)
Cortical bases of speech perception: Evidence from functional lesion studies
Cognition
(2004)- et al.
Neuroperceptual differences in consonant and vowel discrimination: As revealed by direct cortical electrical interference
Cortex
(1997) - et al.
Auditory speech processing in the left temporal lobe: An electrical interference study
Brain and Language
(1995) - et al.
Neuronames brain hierarchy
Neuroimage
(1995) - et al.
Where (in the brain) do semantic errors come from?
Cortex
(2009) - et al.
Differential activation of right and left posterior sylvian regions by semantic and phonological tasks: A positron-emission tomography study in normal human subjects
Neuroscience Letters
(1994) - et al.
Lesion analysis of the brain areas involved in language comprehension
Cognition
(2004) - et al.
Disconnected phonology: A linguistic analysis of phonemic jargon aphasia
Brain and Language
(1996) - et al.
Dorsal and ventral streams: A framework for understanding aspects of the functional anatomy of language
Cognition
(2004) - et al.
The spatial and temporal signatures of word production components
Cognition
(2004)
The nature of the phonological disorder in conduction aphasia
Brain and Language
Semantic memory and the brain: Structure and processes
Current Opinion in Neurobiology
The neurobiology of language and verbal memory: Observations from awake neurosurgery
International Journal of Psychophysiology
Functional specialization for semantic and phonological processing in the left inferior prefrontal cortex
Neuroimage
Functional imaging studies of aphasia
Cognitive neuropsychological analysis and neuroanatomic correlates in a case of acute anomia
Brain and Language
A spreading-activation theory of lemma retrieval in speaking
Cognition
Load-dependent roles of frontal brain regions in the maintenance of working memory
Neuroimage
Effects of repetition and competition on prefrontal activity during word generation
Neuron
Mapping cortical activity elicited with electrical microstimulation using fMRI in the macaque
Neuron
Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing
Neuroimage
Anomia in patients with left inferior temporal lobe lesions
Aphasiology
Human brain language areas identified by functional magnetic resonance imaging
Journal of Neuroscience
Functional neuroimaging of language
Deficits of speech production and speech perception in aphasia
Activation of language cortex with automatic speech tasks
Neurology
Lightweight XML-based query, integration and visualization of distributed, multimodality brain imaging data
Journal of Neuroscience
Target-related neologism formation in jargonaphasia
Brain and Language
Dissociation of action and object naming: Evidence from cortical stimulation mapping
Human Brain Mapping
Neuroanatomical correlates of the aphasia
A neural basis for lexical retrieval
Nature
The role of computational models in neuropsychological investigations of language: Reply to Ruml and Caramazza (2000)
Psychological Review
Anomia: Case studies with lesion localization
Neurocase
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