Learning face perception without vision: Rebound learning effect and hemispheric differences in congenital vs late-onset blindness

Abstract

To address the longstanding questions of whether the blind-from-birth have an innate face-schema, what plasticity mechanisms underlie non-visual face learning, and whether there are interhemispheric face processing differences in face processing in the blind, we used a unique non-visual drawing-based training in congenitally blind (CB), late-blind (LB) and blindfolded-sighted (BF) groups of adults. This Cognitive-Kinesthetic Drawing approach previously developed by Likova (e.g., 2010, 2012, 2013) enabled us to rapidly train and study training-driven neuroplasticity in both the blind and sighted groups. The five-day two-hour training taught participants to haptically explore, recognize, memorize raised-line images, and draw them free-hand from memory, in detail, including the fine facial characteristics of the face stimuli. Such drawings represent an externalization of the formed memory. Functional MRI was run before and after the training. Tactile-face perception activated the occipito-temporal cortex in all groups. However, the training led to a strong, predominantly left-hemispheric reorganization in the two blind groups, in contrast to right-hemispheric in blindfolded-sighted, i.e., the post-training response-change was stronger in the left hemisphere in the blind, but in the right in the blindfolded. This is the first study to discover interhemispheric differences in non-visual face processing. Remarkably, for face perception this learning-based change was positive in the CB and BF groups, but negative in the LB-group. Both the lateralization and inversed-sign learning effects were specific to face perception, but absent for the control nonface categories of small objects and houses. The unexpected inversed-sign training effect in CB vs LB suggests different stages of brain plasticity in the ventral pathway specific to the face category. Importantly, the fact that only after a very few days of our training, the totally-blind-from-birth CB manifested a very good (haptic) face perception, and even developed strong empathy to the explored faces, implies a preexisting face schema that can be "unmasked" and "tuned up" by a proper learning procedure. The Likova Cognitive-Kinesthetic Training is a powerful tool for driving brain plasticity, and providing deeper insights into non-visual learning, including emergence of perceptual categories. A rebound learning model and a neuro-Bayesian economy principle are proposed to explain the multidimensional learning effects. The results provide new insights into the Nature-vs-Nurture interplay in rapid brain plasticity and neurorehabilitation.

Keywords: blindness; drawing training; face learning; lateralization; non-visual learning; plasticity; spatial cognition; tactile memory; training.

Figures

FIG. 1.

Left panel. The fMRI experimental design includes a sequence of five tasks, separated by rest periods. This paper focusses on the “Explore and Memorize” task only (white dashed outline).Right Panel. Examples of the raised-line face images. Initially, the congenitally blind usually had no interest in faces and their structural understanding of face images was quite limited -many were not even able to relate the organization of facial parts to their own faces. Some were wondering how the sighted can enjoy any drawings, as drawings are “flat” images. Thus, it was remarkable when after only the few days of the Cognitive-Kinesthetic Training, they became able to easily recognize and fully understand faces, their appearance, and even facial expressions. Furthermore, some CB developed such strong empathy that refused to work with the ‘unhappy’ face (right, red cross) but liked the ‘happy’, smiling face and didn’t at all mind his boldness (left, green checkmark).

FIG. 2.

To measure the large-scale effect, a large-scale ROI was defined at the occipito-temporal cortex (LSOT; blue outline). The upper panels show the location of the LSOT in the left (A) and right (B) hemispheres. The lower panels show the LSOT on the inflated and rotated to the ventral side surfaces of the left (C) and the right (D) hemispheres. LSOT ~1000 voxels per hemisphere.

FIG. 3.

Average activation maps of the two groups of blindness (CB and LB) and of blindfolded (BF) in the LSOT area of the visual ventral pathway. LSOT region in the left (LH) and right (RH) hemispheres (blue) were defined to measure the large-scale effects. The grey bars represent the pre-training BOLD response bilaterally; the checkerboard bars - the post-training BOLD response. The training effect is measured by the difference between the post-training and pre-training responses. Increased training effects are shown by red bars, and reduced training effects are shown by blue bars. Note the opposite sign effect in the acquired, or late-onset, blindness. The training effect was stronger in the left hemispheres of the blind groups, but in the right hemisphere of the blindfolded-sighted.

FIG. 4.

Sub-divisions of the LSOT are outlined in different colors. Four ROIs are blilaterally symmetrical: LOC (yellow), LOV (white), VT (cyan), and MTV (magenta). The MTas (green) is unique for left hemisphere, and the MTVa (violet) - for the right hemisphere.

FIG. 5.

For each sub-divisional ROI within LSOT, a triplet of bars is shown, representing the BOLD responses (i) pre-training, (ii) post-training and (iii) the change from pre-to-post. The pre-training responses (the first bar in each group) are shown in filled colors, corresponding to the color coding of the respective ROI (see Fig. 4). The post-training signals (second bar) are shown in checkerboard bars. The training-caused change is shown in either red (positive change, enhancement) or in blue (negative change, reduction). LH - Left hemisphere; RH – Right hemisphere.

FIG. 6.

Non-visual training effect in each hemisphere as function of stimulus category (objects, faces and houses) and visual-status group (congenitally blind, CB; late-onset blind, LB; and blindfolded, BF). As above, the triplet of bars represents the BOLD responses: (i) pre-training (gray), (ii) post-training (checkerboard), (iii) change from pre-to-post (color). The training-caused change is shown in either red (positive change, enhancement) or in blue (negative change, reduction). LH - Left hemisphere; RH – Right hemisphere. Note that the inverse learning response for LB vs CB is present only in the face category (second row).

FIG. 7.

We propose a Rebound Learning Model to explain the observed inverted-U curve for learning-driven activation of non-visual face perception. It clearly manifests when comparing (i) a case in which at least one of the variables is new and has not been learned before starting training – e.g., either the perceptual category (as faces in the case of CB) or the use of particular sensory modality (as the use of tactile modality for face perception in the BF), vs. (ii) a case in which all these variables have been already learned and used to some degree, so as they have become “overlearned” after training. This model is inspired by our data on brain activation changes driven by the Cognitive-Kinesthetic face learning (see Figs. 5, 6; Table 1).