Aberrant Modulation of Brain Activity Underlies Impaired Working Memory Following Traumatic Brain Injury

Overview

Journal Neuroimage Clin

Publisher Elsevier

Specialties Neurology
Radiology

Date 2021 Aug 3

PMID 34343728

Citations 1

Authors

Abbie S Taing

Matthew E Mundy

Jennie L Ponsford

Gershon Spitz

Affiliations

Soon will be listed here.

Abstract

Impaired working memory is a common and disabling consequence of traumatic brain injury (TBI) that is caused by aberrant brain processing. However, little is known about the extent to which deficits are perpetuated by specific working memory subprocesses. Using a combined functional magnetic resonance imaging (fMRI) and working memory paradigm, we tested the hypothesis that the pattern of brain activation subserving working memory following TBI would interact with both task demands and specific working memory subcomponents: encoding, maintenance, and retrieval. Forty-three patients with moderate-severe TBI, of whom 25 were in the acute phase of recovery (M = 2.16 months, SD = 1.48 months, range = 0.69 - 6.64 months) and 18 in the chronic phase of recovery (M = 23.44 months, SD = 6.76 months, range = 13.35 - 34.82 months), were compared with 38 demographically similar healthy controls. Behaviourally, we found that working memory deficits were confined to the high cognitive load trials in both acute (P = 0.006) and chronic (P = 0.024) cohorts. Furthermore, results for a subset of the sample (18 chronic TBI and 17 healthy controls) who underwent fMRI revealed that the TBI group showed reduced brain activation when simply averaged across all task trials (regardless of cognitive load or subcomponent). However, interrogation of the subcomponents of working memory revealed a more nuanced pattern of activation. When examined more closely, patterns of brain activity following TBI were found to interact with both task demands and the working memory subcomponent: increased activation was observed during encoding in the left inferior occipital gyrus whereas decreased activation was apparent during maintenance in the bilateral cerebellum and left calcarine sulcus. Taken together, findings indicate an inability to appropriately modulate brain activity according to task demand that is specific to working memory encoding and maintenance.

Citing Articles

The Effect of Traumatic Brain Injury on Memory.

Abdul Razak L, Denis T, Murugiah Y, Yoong W, Idris Z, Senik M Malays J Med Sci. 2024; 31(3):52-74.

PMID: 38984242 PMC: 11229567. DOI: 10.21315/mjms2024.31.3.4.

References

Jensen O, Gelfand J, Kounios J, Lisman J . Oscillations in the alpha band (9-12 Hz) increase with memory load during retention in a short-term memory task. Cereb Cortex. 2002; 12(8):877-82. DOI: 10.1093/cercor/12.8.877. View

Pomarol-Clotet E, Salvador R, Sarro S, Gomar J, Vila F, Martinez A . Failure to deactivate in the prefrontal cortex in schizophrenia: dysfunction of the default mode network?. Psychol Med. 2008; 38(8):1185-93. DOI: 10.1017/S0033291708003565. View

Perlstein W, Cole M, Demery J, Seignourel P, Dixit N, Larson M . Parametric manipulation of working memory load in traumatic brain injury: behavioral and neural correlates. J Int Neuropsychol Soc. 2004; 10(5):724-41. DOI: 10.1017/S1355617704105110. View

Dale A, Fischl B, Sereno M . Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage. 1999; 9(2):179-94. DOI: 10.1006/nimg.1998.0395. View

Sanchez-Carrion R, Fernandez-Espejo D, Junque C, Falcon C, Bargallo N, Roig T . A longitudinal fMRI study of working memory in severe TBI patients with diffuse axonal injury. Neuroimage. 2008; 43(3):421-9. DOI: 10.1016/j.neuroimage.2008.08.003. View

Ramnani N . The primate cortico-cerebellar system: anatomy and function. Nat Rev Neurosci. 2006; 7(7):511-22. DOI: 10.1038/nrn1953. View

Mak L, Minuzzi L, MacQueen G, Hall G, Kennedy S, Milev R . The Default Mode Network in Healthy Individuals: A Systematic Review and Meta-Analysis. Brain Connect. 2016; 7(1):25-33. DOI: 10.1089/brain.2016.0438. View

Pyka M, Beckmann C, Schoning S, Hauke S, Heider D, Kugel H . Impact of working memory load on FMRI resting state pattern in subsequent resting phases. PLoS One. 2009; 4(9):e7198. PMC: 2745698. DOI: 10.1371/journal.pone.0007198. View

McAllister T, Sparling M, Flashman L, Guerin S, Mamourian A, Saykin A . Differential working memory load effects after mild traumatic brain injury. Neuroimage. 2001; 14(5):1004-12. DOI: 10.1006/nimg.2001.0899. View

10.

Narayanan N, Prabhakaran V, Bunge S, Christoff K, Fine E, Gabrieli J . The role of the prefrontal cortex in the maintenance of verbal working memory: an event-related FMRI analysis. Neuropsychology. 2005; 19(2):223-32. DOI: 10.1037/0894-4105.19.2.223. View

11.

Sanchez-Carrion R, Vendrell Gomez P, Junque C, Fernandez-Espejo D, Falcon C, Bargallo N . Frontal hypoactivation on functional magnetic resonance imaging in working memory after severe diffuse traumatic brain injury. J Neurotrauma. 2008; 25(5):479-94. DOI: 10.1089/neu.2007.0417. View

12.

Gerton B, Brown T, Meyer-Lindenberg A, Kohn P, Holt J, Olsen R . Shared and distinct neurophysiological components of the digits forward and backward tasks as revealed by functional neuroimaging. Neuropsychologia. 2004; 42(13):1781-7. DOI: 10.1016/j.neuropsychologia.2004.04.023. View

13.

Sambataro F, Murty V, Callicott J, Tan H, Das S, Weinberger D . Age-related alterations in default mode network: impact on working memory performance. Neurobiol Aging. 2008; 31(5):839-52. PMC: 2842461. DOI: 10.1016/j.neurobiolaging.2008.05.022. View

14.

Tomlinson S, Davis N, Morgan H, Bracewell R . Cerebellar contributions to verbal working memory. Cerebellum. 2013; 13(3):354-61. DOI: 10.1007/s12311-013-0542-3. View

15.

Baddeley A . Working memory. Curr Biol. 2010; 20(4):R136-40. DOI: 10.1016/j.cub.2009.12.014. View

16.

Draper K, Ponsford J . Cognitive functioning ten years following traumatic brain injury and rehabilitation. Neuropsychology. 2008; 22(5):618-625. DOI: 10.1037/0894-4105.22.5.618. View

17.

Rossi A, Pessoa L, Desimone R, Ungerleider L . The prefrontal cortex and the executive control of attention. Exp Brain Res. 2008; 192(3):489-97. PMC: 2752881. DOI: 10.1007/s00221-008-1642-z. View

18.

Hillary F . Neuroimaging of working memory dysfunction and the dilemma with brain reorganization hypotheses. J Int Neuropsychol Soc. 2008; 14(4):526-34. DOI: 10.1017/S1355617708080788. View

19.

Scherf K, Sweeney J, Luna B . Brain basis of developmental change in visuospatial working memory. J Cogn Neurosci. 2006; 18(7):1045-58. DOI: 10.1162/jocn.2006.18.7.1045. View

20.

Abraham A, Pedregosa F, Eickenberg M, Gervais P, Mueller A, Kossaifi J . Machine learning for neuroimaging with scikit-learn. Front Neuroinform. 2014; 8:14. PMC: 3930868. DOI: 10.3389/fninf.2014.00014. View