Shaheen Hamdy

Long-term reorganization of human motor cortex driven by short-term sensory stimulation

Removal of sensory input can induce changes in cortical motor representation that reverse when sensation is restored. Here we ask whether manipulation of sensory input can induce long-term reorganization in human motor cortex that outlasts the initial conditioning. We report that for at least 30 minutes after pharyngeal stimulation, motor cortex excitability and area of representation for the pharynx increased, while esophagus representation decreased, without parallel changes in the excitability of brainstem-mediated reflexes. Therefore increased sensory input can drive long-term cross-system changes in motor areas of the cerebral cortex, which suggests that sensory stimulation might rehabilitate dysphagia, a frequent consequence of cerebral injury.

The cortical topography of human swallowing musculature in health and disease

Because no detailed information exists regarding the topographic representation of swallowing musculature on the human cerebral cortex in health or disease, we used transcranial magnetic stimulation to study the cortical topography of human oral, pharyngeal and esophageal musculature in 20 healthy individuals and the topography of pharyngeal musculature in two stroke patients, one with and one without dysphagia. Our results demonstrate that swallowing musculature is discretely and somatotopically represented on the motor and premotor cortex of both hemispheres but displays interhemispheric asymmetry, independent of handedness. Following stroke, dysphagia appeared to be associated with smaller pharyngeal representation on the intact hemisphere, which increases in size with recovery of swallowing.

Driving Plasticity in Human Adult Motor Cortex Is Associated with Improved Motor Function after Brain Injury

Changes in somatosensory input can remodel human cortical motor organization, yet the input characteristics that promote reorganization and their functional significance have not been explored. Here we show with transcranial magnetic stimulation that sensory-driven reorganization of human motor cortex is highly dependent upon the frequency, intensity, and duration of stimulus applied. Those patterns of input associated with enhanced excitability (5 Hz, 75% maximal tolerated intensity for 10 min) induce stronger cortical activation to fMRI. When applied to acutely dysphagic stroke patients, swallowing corticobulbar excitability is increased mainly in the undamaged hemisphere, being strongly correlated with an improvement in swallowing function. Thus, input to the human adult brain can be programmed to promote beneficial changes in neuroplasticity and function after cerebral injury.

Cortical activation during human volitional swallowing : an event-related fMRI study

Functional magnetic resonance imaging (fMRI) provides a safe, noninvasive method for studying task-related cortical neuronal activity. Because the cerebral cortex is strongly implicated in the control of human swallowing, we sought to identify its functional neuroanatomy using fMRI. In 10 healthy volunteers, a swallow event-related paradigm was performed by injecting 5 ml water bolus into the oral cavity every 30 s. Whole brain functional magnetic susceptibility[Formula: see text]-weighted spiral imaging data were simultaneously acquired over 600 s on a 1.5-T magnetic resonance scanner, utilizing the blood oxygenation level-dependent technique, and correlation maps were generated using both >99% percentile rank and spatial extent thresholding. We observed areas of increased signal change consistently in caudal sensorimotor cortex, anterior insula, premotor cortex, frontal operculum, anterior cingulate and prefrontal cortex, anterolateral and posterior parietal cortex, and precuneus and superiomedial temporal cortex. Less consistent activations were also seen in posterior cingulate cortex and putamen and caudate nuclei. Activations were bilateral, but almost every region, particularly the premotor, insular, and frontal opercular cortices, displayed lateralization to one or the other hemisphere. Swallow-related cortical activity is multidimensional, recruiting brain areas implicated in processing motor, sensory, and attention/affective aspects of the task.

Identification of human brain loci processing esophageal sensation using positron emission tomography

BACKGROUND & AIMS Brain loci that process human esophageal sensation remain unidentified. The aim of this study was to identify the brain loci that process nonpainful and painful human esophageal sensation. METHODS In 8 healthy subjects (7 men; age range, 24-47 years), distal esophageal stimulation was performed by repeatedly inflating a balloon at volumes that produced either no sensation, definite sensation, or pain. Two positron emission tomography scans were performed for each sensation using H2(15)O. Magnetic resonance brain scans were also performed in each subject, and the positron emission tomography data were coregistered with magnetic resonance scans. Analysis of covariance-corrected t images showing the contrasts definite sensation-baseline, pain-baseline, and pain-definite sensation were created. RESULTS Nonpainful stimulation elicited bilateral activations along the central sulcus, insular cortex, and frontal/parietal operculum (P < 0.01). Painful stimulation produced more intense activations of the same areas and additional activation of the right anterior insular cortex and the anterior cingulate gyrus. Multiple areas of decreased activation were also observed; prominent among these was the right prefrontal cortex, which was inhibited during both nonpainful and painful stimulation. CONCLUSIONS Esophageal sensation activates bilaterally the insula, primary somatosensory cortex, and operculum. The right anterior insular cortex and anterior cingulate gyrus process esophageal pain.

Recovery of swallowing after dysphagic stroke relates to functional reorganization in the intact motor cortex

BACKGROUND & AIMS The aim of this study was to determine the mechanism for recovery of swallowing after dysphagic stroke. METHODS Twenty-eight patients who had a unilateral hemispheric stroke were studied 1 week and 1 and 3 months after the stroke by videofluoroscopy. Pharyngeal and thenar electromyographic responses to magnetic stimulation of multiple sites over both hemispheres were recorded, and motor representations were correlated with swallowing recovery. RESULTS Dysphagia was initially present in 71% of patients and in 46% and 41% of the patients at 1 and 3 months, respectively. Cortical representation of the pharynx was smaller in the affected hemisphere (5 +/- 1 sites) than the unaffected hemisphere (13 +/- 1 sites; P </= 0.001). Nondysphagic and persistently dysphagic patients showed little change in pharyngeal representation in either hemisphere at 1 and 3 months compared with presentation, but dysphagic patients who recovered had an increased pharyngeal representation in the unaffected hemisphere at 1 and 3 months (15 +/- 2 and 17 +/- 3 vs. 9 +/- 2 sites; P </= 0.02) without change in the affected hemisphere. In contrast, thenar representation increased in the affected hemisphere but not the unaffected hemisphere at 1 and 3 months (P </= 0.01). CONCLUSIONS Return of swallowing after dysphagic stroke is associated with increased pharyngeal representation in the unaffected hemisphere, suggesting a role for intact hemisphere reorganization in recovery.

Explaining oropharyngeal dysphagia after unilateral hemispheric stroke.

BACKGROUND Oropharyngeal dysphagia occurs in up to a third of patients presenting with a unilateral hemiplegic stroke, yet its neurophysiological basis remains unknown. To explore the relation between cortical motor function of swallowing and oropharyngeal dysphagia, mylohyoid, pharyngeal, and thenar electromyographic responses to stimulation of affected and unaffected hemispheres were recorded in dysphagic and non-dysphagic patients. METHODS The 20 patients studied had unilateral hemispheric stroke confirmed by computed tomography. Eight of them had associated swallowing difficulties. Electromyographic responses were recorded after suprathreshold transcranial magneto-electric stimulation of affected and unaffected hemispheres with a figure-of-eight coil. FINDINGS Stimulation of the unaffected hemisphere evoked smaller pharyngeal responses in dysphagic patients than in non-dysphagic patients (mean 64 microV, median 48, interquartile range 44-86 vs 118 microV, 81, 73-150) (p < 0.02). With stimulation of the affected hemisphere, the pharyngeal responses were smaller than for the unaffected hemisphere but similar between the two patient groups (26 microV, 0, 0-48 vs 54 microV, 0, 0-80). Dysphagic and non-dysphagic patients showed similar mylohyoid and thenar responses to stimulation of the unaffected hemisphere as well as to stimulation of the affected hemisphere-unaffected mylohyoid (269 microV, 239, 89-372 vs 239 microV, 163, 133-307), thenar (572 microV, 463, 175-638 vs 638 microV, 485, 381-764); affected mylohyoid (60 microV, 41, 0-129 vs 96 microV, 0, 0-195); thenar (259 microV, 258, 0-538 vs 451 microV, 206, 8-717). INTERPRETATION The findings indicate that dysphagia after unilateral hemispheric stroke is related to the magnitude of pharyngeal motor representation in the unaffected hemisphere.

Dysphagia in stroke patients.

Swallowing musculature is asymmetrically represented in both motor cortices. Stroke affecting the hemisphere with the dominant swallowing projection results in dysphagia and clinical recovery has been correlated with compensatory changes in the previously non-dominant, unaffected hemisphere. This asymmetric bilaterality may explain why up to half of stroke patients are dysphagic and why many will regain a safe swallow over a comparatively short period. Despite this propensity for recovery, dysphagia carries a sevenfold increased risk of aspiration pneumonia and is an independent predictor of mortality. The identification, clinical course, pathophysiology, and treatment of dysphagia after stroke are discussed in this review.

Modulation of human swallowing behaviour by thermal and chemical stimulation in health and after brain injury.

Abstract Few data support thermal or chemical stimulation as therapy for neurogenic dysphagia. Our aims were to explore the behavioural effects of thermal (cold) and chemical (citrus) modalities on water swallowing in health (n = 65, mean age 45 years, 44 females) and acute stroke (n = 22, mean age 67 years, eight females). Multiple randomized timed 50‐mL swallowing tests were performed for each of four water conditions: (a) room temperature (RT), (b) cold (CD), (c) citrus (CT) and (d) combined cold and citrus (CD + CT). The inter‐swallow interval (ISI), swallowing volume velocity (speed), and volume per swallow (capacity) were measured. In health, compared to RT, only CD + CT slowed the speed (12.3 ± 0.5 vs 10.3 ± 0.5 mL s−1, P < 0.03) and decreased the capacity (16.4 ± 0.9 vs 14.6 ± 0.7 mL per swallow, P < 0.02) of swallowing. ISI was unaffected, except by CD + CT in healthy young subjects (<60 years) where it was reduced (1.44 ± 0.02 vs 1.30 ± 0.02 s, P < 0.02). Despite smaller volumes ingested by stroke patients, CD + CT, compared to RT, again slowed both the speed (3.8 ± 0.4 vs 4.5 ± 0.5 mL s−1, P < 0.03) and capacity (7.6 ± 0.7 vs 8.5 ± 0.7 mL per swallow, P < 0.03) of swallowing but had no effect on ISI. We conclude that combined thermal and chemical modification of water consistently alters swallowing behaviour in health and after cerebral injury. These findings have relevance in the management of neurogenic swallowing problems.

Cortical input in control of swallowing.

Purpose of reviewThis review presents a current synopsis of newer research in cortical control of swallowing and its relationship to advancing knowledge in the field of human swallowing neurophysiology. The intent is to highlight recent findings and to stimulate potential research questions not yet investigated. Recent findingsAdvances in human brain imaging have led to a wealth of newer insights into the cortical and subcortical control of human swallowing. This includes a better understanding of the hemispheric contributions to swallowing control and the mechanisms that underlie recovery or compensation after neurological injury. SummaryThrough advances in imaging and neuroimaging techniques, our knowledge of the neuroanatomy and physiology of swallowing has increased dramatically over the last decade. Integration and interconnection of the diverse swallowing cortical network and how sensory input influences swallowing cortical activation has started to provide a better understanding of the physiological mechanisms that underpin this exquisite yet fundamental sensorimotor function. Experimental paradigms for swallowing neural reorganization have begun to provide evidence for their translation into clinical practice for dysphagia rehabilitation.