Neural Dedifferentiation across the Lifespan in the Motor and Somatosensory Systems

Abstract

Age-related declines in sensorimotor performance have been linked to dedifferentiation of neural representations (i.e., more widespread activity during task performance in older versus younger adults). However, it remains unclear whether changes in neural representations across the adult lifespan are related between the motor and somatosensory systems, and whether alterations in these representations are associated with age declines in motor and somatosensory performance. To investigate these issues, we collected functional magnetic resonance imaging and behavioral data while participants aged 19-76 years performed a visuomotor tapping task or received vibrotactile stimulation. Despite one finding indicative of compensatory mechanisms with older age, we generally observed that 1) older age was associated with greater activity and stronger positive connectivity within sensorimotor and LOC regions during both visuomotor and vibrotactile tasks; 2) increased activation and stronger positive connectivity were associated with worse performance; and 3) age differences in connectivity in the motor system correlated with those in the somatosensory system. Notwithstanding the difficulty of disentangling the relationships between age, brain, and behavioral measures, these results provide novel evidence for neural dedifferentiation across the adult lifespan in both motor and somatosensory systems and suggest that dedifferentiation in these two systems is related.

Keywords: aging; connectivity; dedifferentiation; sensorimotor; task activity.

Figure 1

Associations between age and fMRI activation. (A) Older age was associated with greater recruitment of ipsilateral precentral gyrus during the unimanual (R2R3) tapping condition. Compared to a simpler single-finger condition (R2), a more complex two-finger condition (R2R3) elicited greater recruitment of ipsilateral (B) postcentral gyrus and (C) LOC with older age. (D) Compared to a simpler single-finger condition (R2), a more complex bimanual two-finger condition (R2L2) elicited greater recruitment of right LOC with older age. Numbers under brain images represent MNI coordinates of suprathreshold clusters.

Figure 2

Associations between fMRI activation and motor performance. Increased ipsilateral activation in right (A) precentral gyrus (M1), (B) postcentral gyrus (S1), and (C) lateral occipital cortex (LOC) during R2R3 tapping was associated with an increased duration of the between-finger lag. Blue markers represent participants in their 20s–30s, magenta colors represent participants in their 40s–50s, and red colors represent participants in their 60s–70s. Shaded areas represent the 95% CI.

Figure 3

Associations between fMRI activation and vibrotactile performance outside of the scanner. Increased activation in contralateral LOC, postcentral gyrus, and SMG during R2R3 vibrotactile stimulation was associated with faster tactile simple RTs.

Figure 4

Associations between age and task-based functional connectivity. (A) Older age was associated with positive connectivity between ipsilateral precentral gyrus seed region and lateral occipital cortex (LOC) during R2R3 tapping. (B) Older age was associated with negative connectivity between ipsilateral LOC seed region and superior frontal gyrus during R2R3 tapping. Older age was associated with positive connectivity between left LOC seed region and (C) right LOC during R2R3 vibrotactile stimulation. Yellow colors represent positive associations; green colors represent negative associations.

Figure 5

Associations between connectivity during tactile and motor fMRI tasks. (A) Stronger positive connectivity between right precentral gyrus and right LOC during R2R3 motor tapping was associated with stronger positive connectivity between left LOC and right LOC during R2R3 tactile stimulation. (B) Stronger positive connectivity between right LOC and superior frontal gyrus during R2R3 motor tapping was associated with stronger negative connectivity between left LOC and right LOC during R2R3 tactile stimulation.

Figure 6

Associations between (motor) task-based functional connectivity and motor performance. (A) Stronger positive connectivity between ipsilateral precentral gyrus seed region and lateral occipital cortex (LOC) during R2R3 tapping condition was associated with an increased duration of the between-finger lag. (B) Stronger positive connectivity between ipsilateral LOC seed region and superior frontal gyrus during the intrahemispheric tapping condition was associated with a decreased duration of the between-finger lag.

Figure 7

Associations between (tactile) task-based functional connectivity and vibrotactile performance. Stronger positive connectivity between left LOC seed region with right LOC during R2R3 stimulation was associated with slower (A) simple and (B) choice RTs.