Reduced frontal white matter microstructure in healthy older adults with low tactile recognition performance

Abstract

The aging of the nervous system is a heterogeneous process. It remains a significant challenge to identify relevant markers of pathological and healthy brain aging. A central aspect of aging are decreased sensory acuities, especially because they correlate with the decline in higher cognitive functioning. Sensory and higher cognitive processing relies on information flow between distant brain areas. Aging leads to disintegration of the underlying white matter tracts. While this disintegration is assumed to contribute to higher cognitive decline, data linking structural integrity and sensory function are sparse. The investigation of their interrelation may provide valuable insight into the mechanisms of brain aging. We used a combined behavioral and neuroimaging approach and investigated to what extent changes in microstructural white matter integrity reflect performance declines in tactile pattern recognition with aging. Poor performance in older participants was related to decreased integrity in the anterior corpus callosum. Probabilistic tractography showed that this structure is connected to the prefrontal cortices. Our data point to decreased integrity in the anterior corpus callosum as a marker for advanced brain aging. The correlation between impaired tactile recognition and disintegration in frontal brain networks could provide an explanation why the decrease of sensory function predicts cognitive decline.

Figure 1

Stimulus design and experimental procedure. (A) Braille stimulator. For tactile stimulation, the participants’ right hand was resting on a custom-made board containing a Braille stimulator (QuaeroSys Medical Devices, Schotten, Germany), with the fingertip of the right index finger placed above the stimulating unit. The Braille stimulator consists of eight pins arranged in a four-by-two matrix, each 1 mm in diameter with a spacing of 2.5 mm. Each pin is independently controllable. (B) Stimuli consisted of two sets of four tactile patterns, (C) Sequence of tasks in the experiment, (D) The trial sequence. After a pre-stimulus interval of 1500 ms, tactile patterns were presented to the right index finger with a duration depending on the current step of the experiment. After a wait interval of 1200 ms, a question mark appeared on the screen and participants gave the response via button press. A visual feedback (1000 ms) was provided after every response.

Figure 2

TBSS-Results, FA. TBSS-Results (red), projected on mean-FA-skeleton (green) and mean-FA image. TBSS-Results are thresholded: p < 0.05, FEW-corrected. (A) Y > O-HP, (B) Y > O-LP, (C) O-HP > O-LP, the images are in radiological orientation, coordinates are MNI-coordinates.

Figure 3

Mean FA, AD and RD for O-HP and O-LP in the anterior corpus callosum. (A) mean FA, two-sided t-test, p < 0.001 (O-HP > O-LP), (B) mean AD, two-sided t-test, p = 0.001 (O-HP > O-LP), (C) mean RD, two-sided t-test, p < 0.001 (O-LP > O-HP).

Figure 4

Trajectory map for the resulting tracts for O-HP and O-LP. Superimposed connections resulting from probabilistic tractography on an MNI T1 template for both groups with given z-coordinates. Overlay of binarized group average tracts, thresholded by 50% for both groups. Individual tractography was conducted applying 5000 streamlines per voxel and thresholded by 0.1–2.0% of successful streamlines. The images are all in radiological orientation.