Subcortical functional reorganization due to early blindness

Abstract

Lack of visual input early in life results in occipital cortical responses to auditory and tactile stimuli. However, it remains unclear whether cross-modal plasticity also occurs in subcortical pathways. With the use of functional magnetic resonance imaging, auditory responses were compared across individuals with congenital anophthalmia (absence of eyes), those with early onset (in the first few years of life) blindness, and normally sighted individuals. We find that the superior colliculus, a "visual" subcortical structure, is recruited by the auditory system in congenital and early onset blindness. Additionally, auditory subcortical responses to monaural stimuli were altered as a result of blindness. Specifically, responses in the auditory thalamus were equally strong to contralateral and ipsilateral stimulation in both groups of blind subjects, whereas sighted controls showed stronger responses to contralateral stimulation. These findings suggest that early blindness results in substantial reorganization of subcortical auditory responses.

Keywords: blindness; cross-modal plasticity; medial geniculate nucleus; subcortical pathways; superior colliculus.

Fig. 1.

Auditory stimulation using sparse sampling to minimize scanner acoustical noise: 8-s auditory stimulus (binaural, monaural right, monaural left, and silence) followed by 2 s for volume acquisitions.

Fig. 2.

Example activation across all auditory stimulus conditions (binaural, monaural ipsilateral, and monaural contralateral) for an anophthalmic (A), early blind (B), and sighted control participants [C: Oxford site; D: University of Washington (UW) site]. Statistical maps are thresholded voxelwise at z ≥ 2.5 for visualization purposes.

Fig. 3.

Group activation [in Montreal Neurological Institute (MNI) 2-mm standard space] combined across all auditory stimulus conditions for anophthalmic (A), early blind (B), and sighted control subjects (C: Oxford site; D: UW site). Group statistical maps (mixed effects) are thresholded at z ≥ 2.8 (P < 0.003).

Fig. 4.

Contrasts of anophthalmia > Oxford sighted group (A) and early blind > UW sighted group (B) in all 3 auditory conditions show auditory activity in the expected location of the superior colliculus in blind subjects. Group statistical maps (mixed effects) are thresholded at z ≥ 2.5.

Fig. 5.

Mean %blood oxygenation-level dependent (BOLD) signal change within the superior colliculus during each of the auditory stimulation conditions (binaural, contralateral, and ipsilateral). Results are separated by scan site (A: Oxford site; B: UW site). Error bars represent means ± SE. Note the y-axis scale difference between the 2 sites reflecting the overall reduced response in the UW data.

Fig. 6.

Functional definitions for all subjects (red) are superimposed on the location of anatomically defined medial geniculate nucleus (MGN; blue) and lateral geniculate nucleus (LGN; green). A: anophthalmic group. B: early blind group. C: Oxford control group. D: UW control group.

Fig. 7.

Mean %BOLD change extracted from the auditory thalamus (A: Oxford site; B: UW site) during each of the auditory stimulation conditions (binaural, contralateral and ipsilateral). Error bars represent means ± SE. In the auditory thalamus, both control groups show an attenuated response to ipsilateral auditory stimulation, a pattern not found in either blind group. Note the y-axis scale difference between the 2 sites reflecting the overall reduced response in the UW data.

Fig. 8.

Mean %BOLD change extracted from the inferior colliculus (A: Oxford site; B: UW site) during each of the auditory stimulation conditions (binaural, contralateral, and ipsilateral). Error bars represent means ± SE.

Fig. 9.

Mean %BOLD change within A1 (A: Oxford site; B: UW site) and V1 (C: Oxford site; D: UW site) during each of the auditory stimulation conditions (binaural, contralateral, and ipsilateral). Error bars represent means ± SE.