Elsevier

NeuroImage

Volume 22, Issue 1, May 2004, Pages 68-82
NeuroImage

Functional abnormalities in symptomatic concussed athletes: an fMRI study

https://doi.org/10.1016/j.neuroimage.2003.12.032Get rights and content

Abstract

Our aim was to quantify with functional magnetic resonance imaging (fMRI) changes in brain activity in concussed athletes and compare the results with those of normal control subjects. Regional brain activations associated with a working memory task were obtained from a group of concussed athletes (15 symptomatic, 1 asymptomatic) and eight matched control subjects, using blood oxygen level dependent (BOLD) fMRI. The average percent signal change from baseline to working memory condition in each region of interest was computed. Symptomatic concussed athletes demonstrated task-related activations in some but not all the regions of interest, even when they performed as well as the control subjects. Furthermore, several concussed athletes had additional increases in activity outside the regions of interest, not seen in the control group. Quantitative analysis of BOLD signals within regions of interest revealed that, in general, concussed athletes had different BOLD responses compared to the control subjects. The task-related activation pattern of the one symptom-free athlete was comparable to that of the control group. We also repeated the study in one athlete whose symptoms had resolved. On the first study, when he was still symptomatic, less task-related activations were observed. On follow-up, once his symptoms had disappeared, the task-related activations became comparable to those of the control group. These results demonstrate the potential of fMRI, in conjunction with the working memory task, to identify an underlying pathology in symptomatic concussed individuals with normal structural imaging results.

Introduction

Most studies agree that, of all cases of head trauma, approximately 80% to 90% fall within the category of mild head injury (MHI) or concussion Kraus and Nourjah, 1988, Nell and Brown, 1991, Vazquez-Barquero et al., 1992. Concussion used to be considered as a temporary fluctuation in consciousness without enduring effects on cognition. As such, no long-term sequelae were believed to ensue. Recent cases of athletes and individuals with persistent cognitive deficits following concussion (the post-concussion syndrome) suggest that this is not always the case. Despite being considered as ‘mildly’ injured, individuals who sustain a concussion often exhibit diverse symptomatology and abnormal neuropsychological profiles, such as deficits in working memory, attention, information processing speed, and more generally, in executive function, known to be linked to the frontal lobe Bohnen et al., 1992, Collins et al., 1999, Hinton-Bayre et al., 1997, Leininger et al., 1990, Matser et al., 1999, Newcombe and Briggs, 1994.

Although the exact pathophysiological changes after concussion are not known, there is now increased acceptance of the idea that concussion results mainly in functional disturbance rather than structural damage. This view is reflected in a more comprehensive definition of concussion that was recently proposed by the Concussion in Sport Group(Aubry et al.,2002). According to this updated definition, concussion may be caused either by a direct blow to the head or elsewhere on the body with an ‘impulsive’ force transmitted to the head. Such injury typically results in the rapid onset of short-lived impairment of neurological function that usually resolves spontaneously. Importantly, although concussion may result in neuropathological changes, it is typically associated with grossly normal structural neuroimaging examinations and the acute clinical symptoms largely reflect a functional deficit rather than a structural injury. Thus, functional neuroimaging techniques that examine the metabolic/physiological state of the brain may have great potential for demonstrating brain abnormalities that may be undetectable by morphological imaging methods.

Existing functional imaging studies of individuals with head trauma are mainly based on resting metabolic measurements using positron emission tomography (PET) and single-photon emission computerized tomography (SPECT). Data acquired from these studies have shown perfusion deficits that extend beyond any structural damage shown by CT or MRI Abdel-Dayem et al., 1987, Alavi et al., 1987, Jansen et al., 1996, Langfitt et al., 1986, Newton et al., 1992. The most commonly reported finding is frontal hypometabolism or a decrease in frontal cerebral blood flow. One major disadvantage of these imaging techniques, however, is the requirement of a radioactive tracer, which greatly limits their clinical application. This limitation can be overcome by the relatively new method of functional magnetic resonance imaging (fMRI) which holds great potential for widespread research and clinical use because it does not require exposure to any radioactive substance, has temporal resolution limited only by brain hemodynamics, and spatial resolution comparable to that of conventional MRI. Thus, fMRI can be used both in within and across subjects designs. In a recent fMRI prospective study that used an auditory n-back working memory task with a varying degree of processing load McAllister et al., 1999, McAllister et al., 2001, individuals with mild traumatic brain injury showed a disproportionate increase in activation in right frontal and parietal cortex in response to a moderate working memory demand, but relatively few increases in activation when the working memory load was high.

In the present study, we have used fMRI and a verbal and visual working memory task to test concussed athletes with persisting post concussive symptoms. Our goal was to explore the feasibility of employing functional MRI as a potential diagnostic tool in detecting the effects of concussion and to provide a way to quantify concussive injury. Thus, unlike other functional imaging studies on mild head injury, in which only group comparisons were made, we have examined and quantified the effect of concussion on brain activation patterns at the individual level.

Section snippets

Subjects

Sixteen male athletes (mean age 26.9, SD = 7.2) who had sustained a concussion, ranging from 1 to 14 months before the study (mean = 4.7), and eight normal male control subjects matched in age (mean age 27.6, SD = 5.2) participated in the study. The concussed subjects were elite athletes referred to one of the co-authors (Johnston) at the McGill University Health Center. Data regarding the number of past concussions, the presence/absence of loss of consciousness (LOC) during the last

Behavioral results

Fig. 2 compares the performance of the control and concussed athlete groups on the working memory task. Mixed design ANOVA revealed that the mean performance of the concussed athletes did not differ significantly from that of the control group (F(1,22) = 1.12, P > 0.05). The same analysis indicated that the performance of the two groups was not significantly different on the verbal and visual design versions of the task (F(1,22) = 3.02, P > 0.05), although the concussed athletes seemed to have

Discussion

This study compared functional activation during the performance of a task requiring monitoring of information in working memory in a group of concussed athletes with that of normal control subjects. The control subjects showed strong activation within the mid-dorsolateral prefrontal cortex, consistent with the view that this part of the prefrontal cortex is critical for active monitoring of information in working memory Petrides, 1991, Petrides, 2000a, Petrides, 2000b. The performance of the

Acknowledgements

This project was supported by CIHR operating grant MOP-64271 and grants from the McGill University Health Center and the National Hockey League (Canadian Academy of Sport Medicine/NHL). Dr. K.M. Johnston is supported by the American College of Surgeons Franklin Martin Fellowship. We would like to thank Valentina Petre, André Cormier, and the staff of the McConnell Brain Imaging Centre for support and Rhonda Amsel for valuable comments on statistical analyses of the behavioral data.

References (42)

  • A Alavi et al.

    Positron emission tomography in the evaluation of head injury

    J. Cereb. Blood Flow Metab.

    (1987)
  • M.P Alexander

    Mild traumatic brain injury: pathophysiology, natural history and clinical management

    Neurology

    (1995)
  • M Aubry et al.

    Summary and agreement statement of the 1st International Symposium on Concussion in Sport, Vienna 2001

    Clin. J. Sport Med.

    (2002)
  • N Bohnen et al.

    Neuropsychological deficits in patients with persistent symptoms six months after mild head injury

    Neurosurgery

    (1992)
  • S.H.A Chen et al.

    A study of persistent post-concussion symptoms in mild head trauma using positron emission tomography

    J. Neurol., Neurosurg. Psychiatry

    (2003)
  • M.W Collins et al.

    Relationship between concussion and neuropsychological performance in college football players

    JAMA

    (1999)
  • F Dupuis et al.

    Concussions in athletes produce brain dysfunction as revealed by event-related potentials

    NeuroReport

    (2000)
  • A.I Faden et al.

    The role of excitatory amino acids and NMDA receptors in traumatic brain injury

    Science

    (1989)
  • A.D Hinton-Bayre et al.

    Mild head injury and speed of information processing: a prospective study of professional rugby league players

    J. Clin. Exp. Neuropsychol.

    (1997)
  • H.M.L Jansen et al.

    Cobalt-55 positron emission tomography in traumatic brain injury: a pilot study

    J. Neurol., Neurosurg. Psychiatry

    (1996)
  • B Jennett

    Severity of brain damage. Altered consciousness and other indicators

  • Cited by (0)

    View full text