Functional organization of human sensorimotor cortex for speech articulation

OBJECT The human ventral sensorimotor cortex (vSMC) is involved in facial expression, mastication, and swallowing, as well as the dynamic and highly coordinated movements of human speech production. However, vSMC organization remains poorly understood, and previously published population-driven maps of its somatotopy do not accurately reflect the variability across individuals in a quantitative, probabilistic fashion. The goal of this study was to describe the responses to electrical stimulation of the vSMC, generate probabilistic maps of function in the vSMC, and quantify the variability across individuals. METHODS Photographic, video, and stereotactic MRI data of intraoperative electrical stimulation of the vSMC were collected for 33 patients undergoing awake craniotomy. Stimulation sites were converted to a 2D coordinate system based on anatomical landmarks. Motor, sensory, and speech stimulation responses were reviewed and classified. Probabilistic maps of stimulation responses were generated, and spatial variance was quantified. RESULTS In 33 patients, the authors identified 194 motor, 212 sensory, 61 speech-arrest, and 27 mixed responses. Responses were complex, stereotyped, and mostly nonphysiological movements, involving hand, orofacial, and laryngeal musculature. Within individuals, the presence of oral movement representations varied; however, the dorsal-ventral order was always preserved. The most robust motor responses were jaw (probability 0.85), tongue (0.64), lips (0.58), and throat (0.52). Vocalizations were seen in 6 patients (0.18), more dorsally near lip and dorsal throat areas. Sensory responses were spatially dispersed; however, patients' subjective reports were highly precise in localization within the mouth. The most robust responses included tongue (0.82) and lips (0.42). The probability of speech arrest was 0.85, highest 15–20 mm anterior to the central sulcus and just dorsal to the sylvian fissure, in the anterior precentral gyrus or pars opercularis. CONCLUSIONS The authors report probabilistic maps of function in the human vSMC based on intraoperative cortical electrical stimulation. These results define the expected range of mapping outcomes in the vSMC of a single individual and shed light on the functional organization of the vSMC supporting speech motor control and nonspeech functions.

Download Full-text

Limitations of compensatory plasticity: the organization of the primary sensorimotor cortex in foot-using bilateral upper limb dysplasics

10.1101/190462 ◽

2017 ◽

Cited By ~ 1

Author(s):

Ella Striem-Amit ◽

Gilles Vannuscorps ◽

Alfonso Caramazza

Keyword(s):

Sensorimotor Cortex ◽

Functional Organization ◽

Brain Regions ◽

Association Cortex ◽

Body Parts ◽

Brain Organization ◽

Primary Sensorimotor Cortex ◽

Hand Area ◽

Compensatory Plasticity

SummaryWhat forces direct brain organization and its plasticity? When a brain region is deprived of its input would this region reorganize based on compensation for the disability and experience, or would strong limitations of brain structure limit its plasticity? People born without hands activate their sensorimotor hand region while moving body parts used to compensate for this ability (e.g. their feet). This has been taken to suggest a neural organization based on functions, such as performing manual-like dexterous actions, rather than on body parts. Here we test the selectivity for functionally-compensatory body parts in the sensorimotor cortex of people born without hands. Despite clear compensatory foot use, the sensorimotor hand area in the dysplasic subjects showed preference for body parts whose cortical territory is close to the hand area, but which are not compensatorily used as effectors. This suggests that function-based organization, originally proposed for congenital blindness and deafness, does not apply to cases of the primary sensorimotor cortex deprivation in dysplasia. This is consistent with the idea that experience-independent functional specialization occurs at relatively high levels of representation. Indeed, increased and selective foot movement preference in the dysplasics was found in the association cortex, in the inferior parietal lobule. Furthermore, it stresses the roles of neuroanatomical constraints such as topographical proximity and connectivity in determining the functional development of brain regions. These findings reveal limitations to brain plasticity and to the role of experience in shaping the functional organization of the brain.Significance StatementWhat determines the role of brain regions, and their plasticity when typical inputs or experience is not provided? To what extent can extreme compensatory use affect brain organization? We tested the functional reorganization of the primary sensorimotor cortex hand area in people born without hands, who use their feet for every-day tasks. We found that it is preferentially activated by close-by body-parts which cannot serve as effectors, and not by the feet. In contrast, foot-selective compensatory plasticity was found in the association cortex, in an area involved in tool use. This shows limitations of compensatory plasticity and experience in modifying brain organization of early topographical cortex, as compared to association cortices where function-based organization is the driving factor.ClassificationBiological Sciences\Neuroscience

Download Full-text

An integrated fMRI, SEPs and MEPs approach for assessing functional organization in the malformed sensorimotor cortex

Epilepsy Research ◽

10.1016/j.eplepsyres.2009.12.008 ◽

2010 ◽

Vol 89 (1) ◽

pp. 66-71 ◽

Cited By ~ 3

Author(s):

C. Barba ◽

D. Montanaro ◽

M. Cincotta ◽

F. Giovannelli ◽

R. Guerrini

Keyword(s):

Sensorimotor Cortex ◽

Functional Organization

Download Full-text

A Neuromagnetic Study of the Functional Organization of the Sensorimotor Cortex

European Journal of Neuroscience ◽

10.1111/j.1460-9568.1994.tb00308.x ◽

1994 ◽

Vol 6 (4) ◽

pp. 632-639 ◽

Cited By ~ 56

Author(s):

R. Kristeva-Feige ◽

H. Walter ◽

B. Lütkenhöner ◽

S. Hampson ◽

B. Ross ◽

...

Keyword(s):

Sensorimotor Cortex ◽

Functional Organization

Download Full-text

Can maladaptive cortical plasticity form new sensory experiences? Revisiting phantom pain

Seeing and Perceiving ◽

10.1163/187847612x647667 ◽

2012 ◽

Vol 25 (0) ◽

pp. 134

Author(s):

Tamar R. Makin ◽

Jan Scholz ◽

Nicola Filippini ◽

David Henderson Slater ◽

Irene Tracey ◽

...

Keyword(s):

Functional Connectivity ◽

Sensorimotor Cortex ◽

Cortical Plasticity ◽

Functional Organization ◽

Sensory Deprivation ◽

Limb Amputation ◽

Phantom Pain ◽

Sensory Experiences ◽

Primary Sensorimotor Cortex ◽

Cortical Representations

Phantom pain has become an influential example of maladaptive cortical plasticity. According to this model, sensory deprivation following limb amputation allows for intra-regional invasion of neighbouring cortical representations into the former hand area of the primary sensorimotor cortex, which gives rise to pain sensations. Over the years, this model was extended to explain other disorders of pain, motor control and tinnitus, and has inspired rehabilitation strategies. Yet, other research, demonstrating that phantom hand representation is maintained in the sensorimotor system, and that phantom pain can be triggered by bottom-up aberrant inputs, may call this model to question. Using fMRI, we identified the cortical area representing the missing hand in a group of 18 arm amputees. This allowed us to directly study changes in the ‘phantom’ cortex associated with chronic phantom pain, using functional connectivity and voxel-based morphometry. We show that, while loss of sensory input is generally characterized by structural degeneration of the deprived sensorimotor cortex, the experience of persistent pain was associated with preserved intra-regional structure and functional organization. Furthermore, consistent with the dissociative nature of phantom sensations from other sensory experiences, phantom pain is also associated with reduced long-range inter-regional functional connectivity. We propose that this disrupted inter-regional connectivity may be consequential, rather than causal, of the retained yet isolated local representation of phantom pain. We therefore propose that, contrary to the maladaptive model, cortical plasticity occurs when powerful and long-lasting subjective sensory experience, most likely due to peripheral inputs, is decoupled from the external sensory environment.

Download Full-text