1. A cognitive impairment for sentence planning after
Benjamin L. Chernoff1, Alexander Teghipco1, Frank E. Garcea1, Susan O. Smith2 Webster H. Pilcher2, & Bradford Z. Mahon123
Departments of Brain & Cognitive Sciences1, Neurosurgery2, and Neurology3, University of Rochester
A cognitive impairment for sentence planning after
focal damage to the Frontal Aslant Tract
Background
Neuropsychological Dissociation
Connectivity Changes
Frontal and temporal white-matter pathways have long been implicated in language processing, but the precise functional role of specific tracts is still under investigation. A functional role in verbal fluency has been proposed for a recently described pathway, the Frontal Aslant Tract (FAT), which connects Broca’s area to the pre-supplementary motor area (SMA)1-3
Goal: To understand the functional role of the FAT in sentence planning by longitudinally studying two neurosurgery cases using structural and functional MRI and neuropsychological assessment. Case AF had a left frontal glioma, and case AG had a left hippocampal tumor.
Predictions:
Damage to the FAT to cause dysfluent speech with no anomia, and damage to the inferior longitudinal fasciculus to cause anomia with no dysfluent speech
Corresponding decreases in both functional and structural connectivity between the endpoints of the damaged white matter tracts, not local to the resection
(A) In the Boston Diagnosis of Aphasia Evaluation (BDAE) “Cookie Theft” Test, participants have 2 minutes to describe everything they see in the scene. After tumor resection incidentally damaged the left Frontal Aslant Tract, case AF’s (but not case AG’s) mean length of utterance significantly decreased.
(B) The Snodgrass & Vanderwart (1980) picture naming test requires participants to name black and white line drawings that are balanced for imageability and familiarity. After tumor resection incidentally damaged the left Inferior Longitudinal Fasciculus, case AG’s (but not case AF’s) mean reaction time significantly increased.
(C) We found decreased functional connectivity post-operatively between Broca’s area and the middle/inferior temporal gyrus in case AG (but not case AF)
(D) We found decreased functional connectivity post-operatively between Broca’s area and pre-supplementary motor area A in case AF (but not case AG)
(E) We found significantly decreased mean fractional anisotropy post-operatively in the left Frontal Aslant Tract for case AF (but not case AG)
(F) We found significantly increased mean fractional anisotropy post-operatively in the left inferior longitudinal fasciculus (ILF) for case AG (but not case AF)
Functional MRI Methods
Pre And Post-Operative Tractography
Follow-up Analysis
Stimuli and Design
Experiment 1: Tool, Animal, Face, Place Category Localizer
— 384 Intact and scrambled tool, animal, face, and place stimuli
— 500 ms stimulus presentation within six second miniblock design
Experiment 2: Verbal Fluency
— A cue was presented for either a letter, noun, or action category
— Participants had 30 seconds to overly generate items from that category
Experiment 3: Resting State
— Participants viewed a white fixation cross superimposed on a black screen.
fMRI Scanner Parameters
3T Siemens scanner; 32 channel head coil; TR = 2200 ms, TE = 30 ms; FOV = 384 x 384; 33 slices per volume, 4x4x4 mm voxels; Exp 1: 91 volumes per run, 8 runs; Exp 2: 180 volumes per run, 2 runs each. Analyses were carried out with BrainVoyager and custom MATLAB scripts.
Case AF – Left Frontal Glioma
Case AG – Left Hippocampal Tumor
We observed a grammatical class pattern in spontaneous speech pauses for each case.
For case AF, most of the pauses (9 out of 11) came before a verb or subject of a verb phrase. These pauses were also longer on average. This pattern is consistent with a sentence planning impairment.
For case AG, pauses that came before a noun or noun phrase were longer on average. This pattern is consistent with anomia
Pre-Operative
Tractography
Post-Operative
Tractography
Pre-Operative
Tractography
Post-Operative
Tractography
References:
Chernoff, B.L., Teghipco, A., Garcea, F.E., Sims, M., Paul, D.A., Tivarus, M., Smith, S.O., Pilcher, W.H., ​& Mahon, B.Z. (under review). A role for the Frontal Aslant Tract in speech planning: A neurosurgical case study
Catani, M., Dell’Acqua, F., Vergani, F., Malik, F., Hodge, H., Roy, P., ... Thiebaut de Schotten, M. (2012). Short frontal lobe connections of the human brain. Cortex, 48(2), 273–291.
Mandelli, M. L., Caverzasi, E., Binney, R. J., Henry, M. L., Lobach, I., Block, N., ... Gorno- Tempini, M. L. (2014). Frontal white matter tracts sustaining speech production in primary progressive aphasia. Journal of Neuroscience, 34(29), 9754–9767.
Catani, M., & Thiebaut de Schotten, M. (2008). A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex, 44(8), 1105–1132.
Acknowledgements: We would like to thank Sarah Gannon. This study was funded by NIH grant NS to Brad Mahon, NSF grant to Brad Mahon, and NSF training grant (DGE ) to Benjamin Chernoff
Conclusions
The left Frontal Aslant Tract is a communicative link for sentence planning and lexical access
Lesions to the pre-supplementary motor area can degrade the functional and structural connectivity of Broca’s area
Diffusion MRI Methods
Preprocessing done in FSL: eddy current correction, smoothing of fieldmaps, used for correction of inhomogeneity. Analyses done in FSL using Bayesian estimation of diffusion parameters
Frontal Aslant Tract: Functionally defined 10mm ROI spheres in pre-supplementary motor area and the inferior frontal gyrus.
Inferior Longitudinal Fasciculus: Anatomically constrained ROI’s in the white matter of the occipital lobe on 13 axial slices, and the anterior lobe in 3 axial slices4. An exclusion mask was placed on a coronal slice of the frontal lobe at the edge of the genu
5000 streamlines were sent out from each seed with a curvature threshold of 0.2 and step length of 0.5mm
Left Inferior Longitudinal Fasciculus
Left Frontal Aslant Tract
Right Frontal Aslant Tract