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Comparative Study
. 2011 Jan;68(1):74-84.
doi: 10.1001/archneurol.2010.342.

Deficits in functional connectivity of hippocampal and frontal lobe circuits after traumatic axonal injury

Carlos D Marquez de la Plata  1 , Juanita Garces, Ehsan Shokri Kojori, Jack Grinnan, Kamini Krishnan, Rajesh Pidikiti, Jeffrey Spence, Michael D Devous Sr, Carol Moore, Rodderick McColl, Christopher Madden, Ramon Diaz-Arrastia
Affiliations
Comparative Study

Deficits in functional connectivity of hippocampal and frontal lobe circuits after traumatic axonal injury

Carlos D Marquez de la Plata et al. Arch Neurol. 2011 Jan.

Abstract

Objective: To examine the functional connectivity of hippocampal and selected frontal lobe circuits in patients with traumatic axonal injury (TAI).

Design: Observational study.

Setting: An inpatient traumatic brain injury unit. Imaging and neurocognitive assessments were conducted in an outpatient research facility.

Participants: Twenty-five consecutive patients with brain injuries consistent with TAI and acute subcortical white matter abnormalities were studied as well as 16 healthy volunteers of similar age and sex.

Interventions: Echo-planar and high-resolution T1-weighted images were acquired using 3-T scanners. Regions of interest (ROI) were drawn bilaterally for the hippocampus, anterior cingulate cortex (ACC), and dorsolateral prefrontal cortex and were used to extract time series data. Blood oxygenation level-dependent data from each ROI were used as reference functions for correlating with all other brain voxels. Interhemispheric functional connectivity was assessed for each participant by correlating homologous regions using a Pearson correlation coefficient. Patient functional and neurocognitive outcomes were assessed approximately 6 months after injury.

Main outcome measures: Interhemispheric functional connectivity, spatial patterns of functional connectivity, and associations of connectivity measures with functional and neurocognitive outcomes.

Results: Patients showed significantly lower interhemispheric functional connectivity for the hippocampus and ACC. Controls demonstrated stronger and more focused functional connectivity for the hippocampi and ACC, and a more focused recruitment of the default mode network for the dorsolateral prefrontal cortex ROI. The interhemispheric functional connectivity for the hippocampus was correlated with delayed recall of verbal information.

Conclusions: Traumatic axonal injury may affect interhemispheric neural activity, as patients with TAI show disrupted interhemispheric functional connectivity. More careful investigation of interhemispheric connectivity is warranted, as it demonstrated a modest association with outcome in chronic TBI.

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Figures

Figure 1
Figure 1
Location of Reference Seed Regions of Interest. Note. Location of manually drawn regions of interest. A. Hippocampus. B. Anterior cingulate cortex. C. Left Dorsolateral Prefrontal cortex (radiologic convention).
Figure 2
Figure 2
Bilateral Hippocampal BOLD Fluctuations Over Time. Note. Interhemispheric functional connectivity for left and right hippocampi for a healthy control (above), and for a patient with TAI (below). BOLD signal change is plotted over time. Notice the BOLD signal fluctuates significantly more synchronously in a healthy brain as opposed to an injured brain.
Figure 3
Figure 3
Association between Interhemispheric Hippocampal Connectivity and Verbal Memory Outcome. Note. A Spearman correlation coefficient shows a negative association between interhemispheric hippocampal connectivity and delayed verbal memory. CVLT-II = California Verbal Learning Test-Second Edition.
Figure 4
Figure 4
Figure 4a. Average Left Hippocampus Connectivity among Normal Controls Note for Figures 4a and 4b. A= Hippocampi, B= Basal forebrain, C= Frontal Lobe, D= Hypothalamus, E= Temporal lobe, F= Septal nuclei, G= Subthalamic nuclei, H= parahippocampal gyrus, I= Posterior cingulate. Figure 4b. Average Left Hippocampus Connectivity among Patients with TAI Note: A= Hippocampi, B= Basal forebrain, C= Frontal Lobe, D= Hypothalamus, E= Temporal lobe, F= Septal nuclei, G= Subthalamic nuclei, H= parahippocampal gyrus, I= Posterior cingulate cortex.
Figure 4
Figure 4
Figure 4a. Average Left Hippocampus Connectivity among Normal Controls Note for Figures 4a and 4b. A= Hippocampi, B= Basal forebrain, C= Frontal Lobe, D= Hypothalamus, E= Temporal lobe, F= Septal nuclei, G= Subthalamic nuclei, H= parahippocampal gyrus, I= Posterior cingulate. Figure 4b. Average Left Hippocampus Connectivity among Patients with TAI Note: A= Hippocampi, B= Basal forebrain, C= Frontal Lobe, D= Hypothalamus, E= Temporal lobe, F= Septal nuclei, G= Subthalamic nuclei, H= parahippocampal gyrus, I= Posterior cingulate cortex.
Figure 5
Figure 5
Figure 5a. Average Left Anterior Cingulate Connectivity among Normal Controls Note: Crosshairs were placed on slice closest to midline. A = Right caudate, B= Anterior cingulate cortex, C= Cingulate cortex, D= Posterior cingulate cortex, E = Thalamus, F= Left caudate. Figure 5b: Average Left Anterior Cingulate Connectivity among Patients with TAI Note: Crosshairs were placed on slice closest to midline. A = Right caudate, B= Anterior cingulate cortex, C= Cingulate cortex, D = Posterior cingulate cortex, E = Thalamus, F= Left caudate.
Figure 5
Figure 5
Figure 5a. Average Left Anterior Cingulate Connectivity among Normal Controls Note: Crosshairs were placed on slice closest to midline. A = Right caudate, B= Anterior cingulate cortex, C= Cingulate cortex, D= Posterior cingulate cortex, E = Thalamus, F= Left caudate. Figure 5b: Average Left Anterior Cingulate Connectivity among Patients with TAI Note: Crosshairs were placed on slice closest to midline. A = Right caudate, B= Anterior cingulate cortex, C= Cingulate cortex, D = Posterior cingulate cortex, E = Thalamus, F= Left caudate.
Figure 6
Figure 6
Figure 6a. Average Left Dorsolateral Prefrontal Cortex Connectivity among Normal Controls Note. A = Parahippocampal gyrus, B = Occipito-temporal gyrus, C = Middle temporal gyrus, D = Inferior frontal gyrus, E = Caudate, F = Posterior cingulate cortex, G = Anterior cingulate cortex, H = Angular gyrus, I = Superior frontal gyrus, J = Precuneus. Figure 6b. Average Left Dorsolateral Prefrontal Cortex Connectivity among Patients with TAI Note. A = Parahippocampal gyrus, B = Occipito-temporal gyrus, C = Middle temporal gyrus, D = Inferior frontal gyrus, E = Caudate, F = Posterior cingulate cortex, G = Anterior cingulate cortex, H = Angular gyrus, I = Superior frontal gyrus, J = Precuneus.
Figure 6
Figure 6
Figure 6a. Average Left Dorsolateral Prefrontal Cortex Connectivity among Normal Controls Note. A = Parahippocampal gyrus, B = Occipito-temporal gyrus, C = Middle temporal gyrus, D = Inferior frontal gyrus, E = Caudate, F = Posterior cingulate cortex, G = Anterior cingulate cortex, H = Angular gyrus, I = Superior frontal gyrus, J = Precuneus. Figure 6b. Average Left Dorsolateral Prefrontal Cortex Connectivity among Patients with TAI Note. A = Parahippocampal gyrus, B = Occipito-temporal gyrus, C = Middle temporal gyrus, D = Inferior frontal gyrus, E = Caudate, F = Posterior cingulate cortex, G = Anterior cingulate cortex, H = Angular gyrus, I = Superior frontal gyrus, J = Precuneus.
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