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Neurophysiological Alterations During Strategy-Based Verbal Learning in Traumatic Brain Injury

Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital, Harvard Medical School, Boston, Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Charlestown, strang{at}nmr.mgh.harvard.edu

Richard Goldstein, PhD

Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital, Harvard Medical School, Boston

Therese M. O'Neil-Pirozzi, PhD

Department of Speech-Language Pathology and Audiology, Northeastern University, Boston Massachusetts, Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital, Harvard Medical School, Boston

Kalika Kelkar

Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital, Harvard Medical School, Boston

Christina Supelana, MEd

Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Charlestown

David Burke, MD

Department of Rehabilitation Medicine, Emory University, Atlanta, Georgia

Douglas I. Katz, MD

Department of Neurology, Boston University School of Medicine, Boston, and Braintree Rehabilitation Hospital, Braintree, Massachusetts

Scott L. Rauch, MD

McLean Hospital, Harvard Medical School, Belmont Massachusetts

Cary R. Savage, PhD

Hoglund Brain Imaging Center, Kansas University Medical Center, Kansas City, Kansas

Mel B. Glenn, MD

Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital, Harvard Medical School, Boston

Background. Verbal learning and strategic processing deficits are common sequelae of traumatic brain injury (TBI); however, the neurophysiological mechanisms underlying such deficits remain poorly understood. Methods. We performed functional magnetic resonance imaging (fMRI) in 25 individuals with chronic TBI (>1 year after injury) and 20 matched healthy controls. Subjects were scanned while encoding word lists, with free recall and recognition assessed after each scanning run. To vary the strategic processing load, participants learned semantically unrelated words (Unrelated condition), semantically related words under null instruction conditions (Spontaneous condition), and semantically related words following training on the use of a semantic clustering strategy (Directed condition). Results. Behavioral performance on recall, recognition, and semantic clustering improved significantly as follows: Unrelated < Spontaneous < Directed. Individuals with TBI exhibited impaired yet parallel behavioral performance relative to control participants. The fMRI measures of brain activity during verbal encoding revealed decreased activity in participants with TBI relative to controls in left dorsolateral prefrontal cortex (DLPFC; BA 9) and in a region spanning the left angular and supramarginal gyri (BA 39/40). Functional connectivity analysis revealed evidence of a functional—but not anatomical—breakdown in the connectivity between the DLPFC and other regions specifically when participants with TBI were directed to use the semantic encoding strategy. Conclusion. After TBI, the DLPFC appears to be decoupled from other active brain regions specifically when strategic control is required. We hypothesize that approaches designed to help re-couple DLPFC under such conditions may aid TBI cognitive rehabilitation.

Key Words: Cognitive rehabilitation • Functional neuroimaging • Behavioral neurology • Semantic clustering • Brain trauma

This version was published on March 1, 2009

Neurorehabilitation and Neural Repair, Vol. 23, No. 3, 226-236 (2009)
DOI: 10.1177/1545968308324225


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