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A two-part preliminary investigation of encoding-related activation changes after moderate to severe traumatic brain injury: hyperactivation, repetition suppression, and the role of the prefrontal cortex

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Abstract

Traumatic brain injury (TBI) survivors typically exhibit significant learning and memory deficits and also frequently demonstrate hyperactivation during functional magnetic resonance imaging (fMRI) tasks involving working memory encoding and maintenance. However, it remains unclear whether the hyperactivation observed during such working memory tasks is also present during long-term memory encoding. The preliminary experiments presented here were designed to examine this question. In Experiment 1, 7 healthy controls (HC) and 7 patients with moderate to severe TBI encoded ecologically relevant object location associations (OLA) while undergoing fMRI and then completed a memory test outside of the fMRI environment. fMRI data analysis included only the correctly encoded trials and revealed hyperactivation in the TBI relative to HC group in regions critical for OLA encoding, including bilateral dorsal and ventral visual processing areas, bilateral frontoparietal working memory network regions, and the left medial temporal lobe. There was also an incidental finding that this hyperactivation persisted after multiple exposures to the same stimulus, which may indicate an attenuated repetition suppression effect that could ultimately contribute to cognitive fatigue and inefficient memory encoding after TBI. Experiment 2 directly assessed repetition suppression in some of the same HC and TBI participants. During early encoding trials, the TBI group showed large areas of hyperactivation in the right prefrontal cortex and bilateral posterior parietal cortices relative to the HC. Following additional exposure to these stimuli, the TBI group showed repetition suppression in visual and spatial processing regions, but continued to show hyperactivation in the right dorsolateral prefrontal cortex. Findings from these preliminary studies may reflect that increased reliance on cognitive control mechanisms following TBI extends to memory encoding.

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Acknowledgments

We would like to thank Dr. Felicia Goldstein and Dr. Suzanne Penna for their assistance with participant recruitment. Authors M. Meredith Gillis and Benjamin M. Hampstead have no conflict of interest. This research was supported by funding from the Department of Veterans Affairs, Veterans Health Administration, Office of Research and Development, and Rehabilitation Research and Development Service (grant B6366W to BMH). The contents of this manuscript do not represent the views of the Department of Veterans Affairs or the United States Government.

Conflict of Interest

M. Meredith Gillis and Benjamin M. Hampstead declare that they have no conflicts of interest.

Informed Consent

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation. Informed consent was obtained from all patients for being included in the study.

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  1. Benjamin M. Hampstead

    Present address: Neuropsychology Section, Department of Psychiatry, University of Michigan, 2101 Commonwealth Blvd Suite C, Ann Arbor, MI, 48105, USA

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  1. Rehabilitation R&D Center of Excellence, Atlanta VAMC, 1670 Clairmont Road (151R), Decatur, GA, 30033, USA

    Benjamin M. Hampstead

  2. Department of Rehabilitation Medicine, Emory University School of Medicine, Center for Rehabilitation Medicine, 1441 Clifton Road NE, Atlanta, GA, 30322, USA

    M. Meredith Gillis & Benjamin M. Hampstead

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Gillis, M.M., Hampstead, B.M. A two-part preliminary investigation of encoding-related activation changes after moderate to severe traumatic brain injury: hyperactivation, repetition suppression, and the role of the prefrontal cortex. Brain Imaging and Behavior 9, 801–820 (2015). https://doi.org/10.1007/s11682-014-9337-5

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