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Functional significance of the electrocorticographic auditory responses in the premotor cortex.

ABSTRACT: Other than well-known motor activities in the precentral gyrus, functional magnetic resonance imaging (fMRI) studies have found that the ventral part of the precentral gyrus is activated in response to linguistic auditory stimuli. It has been proposed that the premotor cortex in the precentral gyrus is responsible for the comprehension of speech, but the precise function of this area is still debated because patients with frontal lesions that include the precentral gyrus do not exhibit disturbances in speech comprehension. We report on a patient who underwent resection of the tumor in the precentral gyrus with electrocorticographic recordings while she performed the verb generation task during awake brain craniotomy. Consistent with previous fMRI studies, high-gamma band auditory activity was observed in the precentral gyrus. Due to the location of the tumor, the patient underwent resection of the auditory responsive precentral area which resulted in the post-operative expression of a characteristic articulatory disturbance known as apraxia of speech (AOS). The language function of the patient was otherwise preserved and she exhibited intact comprehension of both spoken and written language. The present findings demonstrated that a lesion restricted to the ventral precentral gyrus is sufficient for the expression of AOS and suggest that the auditory-responsive area plays an important role in the execution of fluent speech rather than the comprehension of speech. These findings also confirm that the function of the premotor area is predominantly motor in nature and its sensory responses is more consistent with the "sensory theory of speech production," in which it was proposed that sensory representations are used to guide motor-articulatory processes.

SUBMITTER: Tanji K

PROVIDER: S-EPMC4360713 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Functional significance of the electrocorticographic auditory responses in the premotor cortex.

Tanji Kazuyo K Sakurada Kaori K Funiu Hayato H Matsuda Kenichiro K Kayama Takamasa T Ito Sayuri S Suzuki Kyoko K

Frontiers in neuroscience 20150316

Other than well-known motor activities in the precentral gyrus, functional magnetic resonance imaging (fMRI) studies have found that the ventral part of the precentral gyrus is activated in response to linguistic auditory stimuli. It has been proposed that the premotor cortex in the precentral gyrus is responsible for the comprehension of speech, but the precise function of this area is still debated because patients with frontal lesions that include the precentral gyrus do not exhibit disturban ...[more]

PMID: 25852457

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Project description:Current models of cortical speech and language processing include multiple regions within the temporal lobe of both hemispheres. Human communication, by necessity, involves complex interactions between regions subserving speech and language processing with those involved in more general cognitive functions. To assess these interactions, we utilized an ecologically salient conversation-based approach. This approach mandates that we first clarify activity patterns at the earliest stages of cortical speech processing. Therefore, we examined high gamma (70-150 Hz) responses within the electrocorticogram (ECoG) recorded simultaneously from Heschl's gyrus (HG) and lateral surface of the superior temporal gyrus (STG). Subjects were neurosurgical patients undergoing evaluation for treatment of medically intractable epilepsy. They performed an expanded version of the Mini-mental state examination (MMSE), which included additional spelling, naming, and memory-based tasks. ECoG was recorded from HG and the STG using multicontact depth and subdural electrode arrays, respectively. Differences in high gamma activity during listening to the interviewer and the subject's self-generated verbal responses were quantified for each recording site and across sites within HG and STG. The expanded MMSE produced widespread activation in auditory cortex of both hemispheres. No significant difference was found between activity during listening to the interviewer's questions and the subject's answers in posteromedial HG (auditory core cortex). A different pattern was observed throughout anterolateral HG and posterior and middle portions of lateral STG (non-core auditory cortical areas), where activity was significantly greater during listening compared to speaking. No systematic task-specific differences in the degree of suppression during speaking relative to listening were found in posterior and middle STG. Individual sites could, however, exhibit task-related variability in the degree of suppression during speaking compared to listening. The current study demonstrates that ECoG recordings can be acquired in time-efficient dialog-based paradigms, permitting examination of language and cognition in an ecologically salient manner. The results obtained from auditory cortex serve as a foundation for future studies addressing patterns of activity beyond auditory cortex that subserve human communication.

Project description:BackgroundThe auditory efferent system has unique neuroanatomical pathways that connect the cerebral cortex with sensory receptor cells. Pyramidal neurons located in layers V and VI of the primary auditory cortex constitute descending projections to the thalamus, inferior colliculus, and even directly to the superior olivary complex and to the cochlear nucleus. Efferent pathways are connected to the cochlear receptor by the olivocochlear system, which innervates outer hair cells and auditory nerve fibers. The functional role of the cortico-olivocochlear efferent system remains debated. We hypothesized that auditory cortex basal activity modulates cochlear and auditory-nerve afferent responses through the efferent system.Methodology/principal findingsCochlear microphonics (CM), auditory-nerve compound action potentials (CAP) and auditory cortex evoked potentials (ACEP) were recorded in twenty anesthetized chinchillas, before, during and after auditory cortex deactivation by two methods: lidocaine microinjections or cortical cooling with cryoloops. Auditory cortex deactivation induced a transient reduction in ACEP amplitudes in fifteen animals (deactivation experiments) and a permanent reduction in five chinchillas (lesion experiments). We found significant changes in the amplitude of CM in both types of experiments, being the most common effect a CM decrease found in fifteen animals. Concomitantly to CM amplitude changes, we found CAP increases in seven chinchillas and CAP reductions in thirteen animals. Although ACEP amplitudes were completely recovered after ninety minutes in deactivation experiments, only partial recovery was observed in the magnitudes of cochlear responses.Conclusions/significanceThese results show that blocking ongoing auditory cortex activity modulates CM and CAP responses, demonstrating that cortico-olivocochlear circuits regulate auditory nerve and cochlear responses through a basal efferent tone. The diversity of the obtained effects suggests that there are at least two functional pathways from the auditory cortex to the cochlea.

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Functional significance of the electrocorticographic auditory responses in the premotor cortex.

Publications

Functional significance of the electrocorticographic auditory responses in the premotor cortex.

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