TITLE:
What can fMRI tell us about swallowing? ”

Georgia A. Malandraki, Ph.D., CCC-SLP

Is swallowing a reflex?

Until recently, the medical field claimed that swallowing is an automatic reflex mediated by the brainstem and does not require brain input to be successfully completed. Thus, it was common for a medical professional to believe that if a patient lost the ability to swallow (e.g. after a severe stroke), they could not easily regain that ability. Imagine how devastating this news could be for thousands of patients suffering from such conditions.

Recent work of neuroscientists including work from our laboratory, however, has now shown that swallowing is NOT a mere reflex, BUT a complex process that depends on the coordination of sensory receptors, muscles, nerves, and the brain and has both automatic and voluntary components. Indeed, we now refer to swallowing as a patterned response, i.e., a response triggered at the level of the brainstem, but patterned or mediated by the brain. How did we learn this information?

Some of the first evidence on the role of the brain in swallowing came from our patients. Early work of JoAnne Robbins’s group showed that even a unilateral cortical stroke (not involving the brainstem) might result in dysphagia [1], opening our eyes to the possibility that the brain must be somehow involved! This was later confirmed by other research [2-4].

More recent evidence on how important the brain is in swallowing is now also stemming from neuroimaging research. The use of a technique known as task functional MRI (fMRI) in many studies has proved important in providing evidence for the complex neural control of swallowing.

What is task fMRI?

In simple terms, task fMRI is a type of MRI that provides indirect information on how the brain works. To understand this better, let’s take a look at the image below.

 

 

Image 1

When a sensory or motor process happens, for example when you are having a memory, or you are swallowing (Image 1.A), areas in the brain that are responsible for that process become neurally active (Image1.B]). When a brain area is neurally active, its gray matter exhibits an increase in the metabolic rate of oxygen and glucose, and subsequently there is an increase in blood flow in that area (Image 1.C). The increase in blood flow further causes a decrease in specialized red blood cells, which has been found to be more paramagnetic than the brain itself. This enables the MR magnet to detect brain activity. Finally, the cool looking images we see in fMRI studies (Image 1.D) are nothing more or less than statistical maps that show us in yellow and red which areas of the brain are more significantly active than the rest of the brain during a specific task.

How can we use fMRI to learn about swallowing, dysphagia and swallowing rehabilitation?

Task-fMRI and swallowing

Task fMRI has been extensively used to help us learn how the brain functions during normal swallowing in healthy adults. From experiments conducted by many research groups, we discovered that a plethora of brain areas are active when people swallow. Some of the most commonly reported areas include: the primary motor and sensory cortices, the frontal operculum, the premotor area, the insula, the anterior cingulate gyrus, as well as areas in the basal ganglia and the thalamus. [5-10] Some of these areas (basal ganglia, insula) have been found to be more related to pharyngeal components of swallowing (such as laryngeal closure) that are more automatic in nature; whereas other areas (primary motor and sensory cortices, premotor area) are considered more important for oral components of swallowing (such as tongue elevation) that are more voluntary in nature [8] (Image 2, with permission).

 

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Image 2

The use of fMRI in understanding the brain in patients with dysphagia has been limited for several reasons. One is the increased difficulty these patients face while swallowing in the supine position (necessary for imaging in the magnet). Additionally, MRI requires patients to lie flat on their back for several minutes, making it challenging for patients with postural restrictions to participate.

Similar to fMRI studies in dysphagia, swallowing treatment fMRI studies are limited. However, an increasing need for use of treatments that are evidence-based is emerging. And one of the highest levels of evidence that can be provided for swallowing treatments is through the use of neuroimaging used in pre- and post-treatment designs.

To elucidate how task fMRI can be used in such a design, we conducted a case study and used fMRI before and after an 8-week lingual strengthening program in a chronic stroke patient. [11] Our preliminary results indicated a dramatic increase in brain activity post-treatment in this patient, who had no other apparent changes in treatment or medication use during this 8-week period, and likely indicate treatment-related plasticity (Image 3). These results, however, should be interpreted with caution, since this is a single subject observation. This study, however, provides an excellent example of what task fMRI can teach us about swallowing rehabilitation.

 

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Image 3

 

Resting-state fcMRI and swallowing

Because task-fMRI can be challenging for patients with dysphagia, we are now in search for alternative methods to study brain function in these patients. A relatively new method, known as resting-state functional connectivity MRI (resting-state fcMRI) permits the investigation of temporal connectivity between functionally connected brain areas during rest. In essence this technology allows us to see how distinct, but functionally connected, brain areas “communicate” with each other at rest. And yes, our brain areas DO communicate with each other, even when we are resting! By using resting-state fcMRI we can indirectly study the integrity of the swallowing network and correlate it with swallowing behavioral measurements that can be elicited outside the magnet. This can have significant practical applications for our field!

Indeed, resting-state fcMRI allowed us to start looking at the connectivity of the swallowing network areas in a group of patients with mild Alzheimer’s Disease (AD). Specifically, we were able to examine the integrity of this connectivity and see that although it is intact in healthy elders, it seems to be compromised in early AD patients with mild swallowing deficits. [12] While we are continuing this line of research in collaboration with the University of Wisconsin in Madison, our laboratory team has now started collecting resting fMRI data on another important but deceivingly understudied patient group, children with cerebral palsy.These children exhibit different degrees and extent of brain lesions and despite these, most of them develop immature but impressive compensatory swallowing skills. The extraordinary neuroplasticity that some of these children exhibit (and we are now starting to examine) may help us better diagnose and treat them, as well as better understand other patients who acquire similar lesions in adulthood. Although it would be almost impossible to use task fMRI to study the neurophysiology of these patents’ population, resting fMRI allows us to do it without any difficulty!

Conclusion

Overall task and resting fMRI is a powerful, non-invasive method (one of many) that has increased our understanding of how the brain works in normal and disordered swallowing and is helping us examine if our treatments are effective in changing our patients’ swallowing as well as brain function! Most important of all, it has confirmed that our brain is plastic and we, as swallowing specialists, can and should take advantage of this knowledge in order to rehabilitate our patients’ swallowing and help them lead better lives.

References

[1] Robbins J, Levin RL. Swallowing after unilateral stroke of the cerebral cortex: preliminary experience. Dysphagia 1988. 311–17.

[2] Daniels SK, Ballo LA, Mahoney MC, Foundas AL. Clinical predictors of dysphagia and aspiration risk: outcome measures in acute stroke patients. Arch Phys Med Rehabil 2000. 81(8): 1030–1033.

[3] Mann G, Hankey G J, Cameron D. Swallowing disorders following acute stroke: prevalence and diagnostic accuracy. Cerebrovasc Dis 2000. 10(5):380–386.

[4] Smithard D G, O’Neill P A, Park C, Morris J. Complications and outcome after acute stroke: Does dysphagia matter? Stroke 1996. 27(7):1200–1204.

[5] Mosier KM, Liu WC, Maldjian JA, Shah R, Modi B. Lateralization of cortical function in swallowing: a functional MR imaging study. AJNR Am J Neuroradiol 1999. 20:1520–1526.

[6] Martin RE, Goodyear BG, Gati JS, Menon RS. Cerebral cortical representation of automatic and volitional swallowing in humans. J Neurophysiol 2001. 85:938–950.

[7] Humbert IA, Fitzgerald ME, McLaren DG, et al. Neurophysiology of swallowing: effects of age and bolus type. Neuroimage 2009. 44:982–991.

[8] Malandraki GA, Sutton BP, Perlman AL, Karampinos DC, Conway C. Neural activation of swallowing and swallowing-related tasks in healthy young adults: an attempt to separate the components of deglutition. Hum Brain Mapp 2009. 30:3209–3226.

[9] Hamdy S, Mikulis DJ, Crawley A, et al. Cortical activation during human volitional swallowing: an event-related fMRI study. Am J Physiol 1999. 277: G219–G225.

[10] Malandraki GA, Sutton BP, Perlman AL, Karampinos DC. Reduced somatosensory activations in swallowing with age. Hum Brain Mapp 2011. 32:730–743.

[11] Malandraki GA, Johnson S, Robbins J. Functional Magnetic Resonance Imaging of swallowing function: From neurophysiology to neuroplasticity. Head and Neck 20011. 33Suppl 1, S14-20.

[12] Malandraki GA, Nair VA, Hind J, Prabhakaran V, Lye YH, Robbins J (2013). Resting-state functional connectivity MRI of swallowing network areas: Preliminary differences between healthy elders and patients with mild Alzheimer’s disease. Annual Dysphagia Research Society Meeting in Seattle, WA (March 14-16, 2013).

 

LEGENDS OF IMAGES:

Image 1: How task fMRI works? Adapted from Dr. John Georgiadis, University of Illinois.

Image 2: Areas of most significant activation during swallowing (shown in red), during throat clearing (shown in blue), and during tongue tapping (shown in yellow). Boxes report the areas. Images are shown in radiological convention (the right hemisphere is shown on the left). Coordinates are given in Montreal Neurological Institute (MNI) space.

(In: Malandraki et al. 2009; used with permission from John Wiley & Sons, Inc.).

Image 3: Brain activity during liquid swallows pre and post lingual strengthening treatment. Adapted from: Malandraki, Johnson, Robbins, 2011.

 

BIO

MalandrakiBio

Dr. Malandraki is currently an Assistant Professor at the Department of Biobehavioral Sciences at Teachers College, Columbia University and the Director of the Swallowing, Voice and Neuroimaging Laboratory and the Dysphagia Research Clinic of Columbia University. Her research focuses on: a) the use of advanced neuro-imaging to understand the neural underpinnings of swallowing components in the normal population and following trauma or intervention and b) the application of telemedicine systems to test the effectiveness of providing speech and swallowing services over the internet.

Beginning in the fall of 2014, Dr. Malandraki will be joining the faculty of Purdue University, where she will continue her line of clinical research and academic work.

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