Crossmodal Connections of Primary Sensory Cortices Largely Vanish During Normal Aging.

Julia U. Henschke,Eike Budinger,Frank W. Ohl

doi:10.3389/fnagi.2018.00052

Abstract

During aging, human response times (RTs) to unisensory and crossmodal stimuli decrease. However, the elderly benefit more from crossmodal stimulus representations than younger people. The underlying short-latency multisensory integration process is mediated by direct crossmodal connections at the level of primary sensory cortices. We investigate the age-related changes of these connections using a rodent model (Mongolian gerbil), retrograde tracer injections into the primary auditory (A1), somatosensory (S1), and visual cortex (V1), and immunohistochemistry for markers of apoptosis (Caspase-3), axonal plasticity (Growth associated protein 43, GAP 43), and a calcium-binding protein (Parvalbumin, PV). In adult animals, primary sensory cortices receive a substantial number of direct thalamic inputs from nuclei of their matched, but also from nuclei of non-matched sensory modalities. There are also direct intracortical connections among primary sensory cortices and connections with secondary sensory cortices of other modalities. In very old animals, the crossmodal connections strongly decrease in number or vanish entirely. This is likely due to a retraction of the projection neuron axonal branches rather than ongoing programmed cell death. The loss of crossmodal connections is also accompanied by changes in anatomical correlates of inhibition and excitation in the sensory thalamus and cortex. Together, the loss and restructuring of crossmodal connections during aging suggest a shift of multisensory processing from primary cortices towards other sensory brain areas in elderly individuals.

Highlights

Multisensory integration recruits higher-level association cortex, and low-level and even primary sensory cortices like the primary auditory (A1), somatosensory (S1), and visual cortex (V1)
We focused on sensory structures of the cortex and thalamus; namely, the primary and secondary sensory cortices and the sensory thalamic nuclei
The General Cyto- and Myeloarchitecture of the Sensory Cortex and Thalamus Do Not Change Over Age

Summary

Introduction

Multisensory integration recruits higher-level association cortex, and low-level and even primary sensory cortices like the primary auditory (A1), somatosensory (S1), and visual cortex (V1) Neurons in these brain regions respond to their own (‘‘matched’’) sensory modality and to other (‘‘non-matched’’) modalities and they receive convergent anatomical inputs from multiple senses (for review, e.g., Schroeder and Foxe, 2005; Driver and Noesselt, 2008; Stein and Stanford, 2008; Budinger and Scheich, 2009; Murray et al, 2016; Meredith and Lomber, 2017). Psychophysical studies have shown that older adults typically have longer RTs to unimodal and crossmodal stimuli but their RT benefit for crossmodal vs unimodal stimuli is larger than for younger adults (for review, e.g., Mozolic et al, 2012; Freiherr et al, 2013; de Dieuleveult et al, 2017). Three different, but not mutually exclusive, mechanisms have been suggested (for review, e.g., Mozolic et al, 2012; Freiherr et al, 2013; de Dieuleveult et al, 2017):

Results

Discussion

Conclusion