Drawing enhances cross-modal memory plasticity in the human brain: a case study in a totally blind adult

Abstract

In a memory-guided drawing task under blindfolded conditions, we have recently used functional Magnetic Resonance Imaging (fMRI) to demonstrate that the primary visual cortex (V1) may operate as the visuo-spatial buffer, or "sketchpad," for working memory. The results implied, however, a modality-independent or amodal form of its operation. In the present study, to validate the role of V1 in non-visual memory, we eliminated not only the visual input but all levels of visual processing by replicating the paradigm in a congenitally blind individual. Our novel Cognitive-Kinesthetic method was used to train this totally blind subject to draw complex images guided solely by tactile memory. Control tasks of tactile exploration and memorization of the image to be drawn, and memory-free scribbling were also included. FMRI was run before training and after training. Remarkably, V1 of this congenitally blind individual, which before training exhibited noisy, immature, and non-specific responses, after training produced full-fledged response time-courses specific to the tactile-memory drawing task. The results reveal the operation of a rapid training-based plasticity mechanism that recruits the resources of V1 in the process of learning to draw. The learning paradigm allowed us to investigate for the first time the evolution of plastic re-assignment in V1 in a congenitally blind subject. These findings are consistent with a non-visual memory involvement of V1, and specifically imply that the observed cortical reorganization can be empowered by the process of learning to draw.

Keywords: blind; brain plasticity; drawing; fMRI; learning; primary visual cortex V1; visuo-spatial sketchpad; working memory.

Figures

Figure 1

Matisse: Lithographs No. 54: “Marie” (left), No. 35: “Ma Maîtresse” (center), No. 45: “Les Colombes Amoureuses” (right), from the illustrations for Ronsard's “Florilège des Amours” (1948).

Figure 2

Experimental design. Drawing was investigated in a three-phase paradigm consisting of a memory-guided drawing task, abbreviated as “MemoryDraw” (MD), plus two control tasks: a motor and “negative” memory control task “Scribble” (S), and a task of perceptual exploration and memorization of the model to be drawn “Explore/Memorize” (E/M). Each task duration was 20 s, with 20 s rest intervals elapsing between the tasks, with the whole trial sequence being repeated 12 times in each scanning session.

Figure 3

Raised-line drawing models. Realistic faces and objects explored by the subject using her left hand in the E/M task were drawn from memory in the MD task after a 20 s rest interval. Two repetitions of each of the six stimuli were run in each fMRI session for total of 12 runs per session.

Figure 4

A subject on the scanner bed operating our novel multimodal MRI-compatible drawing device. The plexiglass gantry supports a drawing tablet while a fiber-optic drawing stylus captures and records the drawing movements with high precision. The motion capture information synchronized with the fMRI allows the effect of behavioral events to be analyzed.

Figure 5

Primary visual cortex shows the predominant learning effect in the MD task. A voxel-wise comparison, projected on inflated representations of the posterior left (LH) and right (RH) hemispheres, shows the increase (orange-yellow coloration) of the post-training BOLD activation in MD relative to the pre-training level. Dark gray, sulci; light gray, gyri.

Figure 6

V1 activation in MD before training (A) and after training (B). BOLD activation (orange-yellowish coloration) from the MD task, derived according to the GLM described in Materials and Methods, and projected on inflated representations of the posterior left (LH) and right (RH) hemispheres is shown for both the pre-training (A) and the post-training (B) fMRI sessions. Medial views of the posterior part of the brain optimally visualize area V1 (green outlines) along the calcarine sulcus. Scale bars show the color-coding for the z-score levels of the activation. Comparison of the pre- to post-training responses shows a dramatic enhancement from negligible activation in V1 before training (A), to a massive task-specific activation as a result of training (B). Note that, interestingly, the extension of the post-training activation approximately corresponds to the spatial extent of the images (∼10° diameter).

Figure 7

Pre/post-training comparison of V1 activation pattern across the three tasks. (A) There was no task-specificity in V1 before training. (B) Remarkably, a clear specialization for MD (red) emerged after training. Bar-graphs show the estimated activation in each hemisphere for each task—E/M, MD, S. The activation levels refer to the beta weights for the event types in the GLM. The dashed lines and the error bars represent confidence intervals for two different forms of statistical comparison of the activation levels. The dashed lines represent the 99% “zero” confidence interval, within which the activations are not significantly different from zero. The error bars are 99% “difference” confidence intervals designed to illustrate the t-test to assess the significance of the differences between activation levels in each figure, i.e., the amplitude differences are not significant unless they exceed the confidence intervals for both compared activations.

Figure 8

Response waveform analysis in V1. The average time courses of BOLD activity (black lines) are shown for the sequence of the three task intervals (white bars); the four dark-gray bars indicate the 20 s rest intervals separating E/M, MD, and S tasks. Immature and non-specific transient “bursts” before the CK-training (A), were transformed after training (B) into well-developed waveforms for the memory-drawing MD, in contrast to the loss of any significant response for the non-memory drawing S.

Figure 9

Response waveform analysis in motor cortex. In contrast to area V1, the LH motor cortex M1 (in particular, the region encoding right-hand movement) produced well-formed response waveforms both before training (in A) and after training (in B). As should be expected, these responses were strong and positive for the two right-hand tasks (MD and S), and zero to negative for the left-hand task (E/M). Statistics as in Figure 7, and Materials and Methods.

Figure 10

Representative examples of pre- vs. post-training drawings. The left panels show the respective raised-line models to be drawn. Note the significant advance from practically unrecognizable drawings before training (middle panels) to well-recognizable drawings achieved by this totally blind subject as a result of the Cognitive-Kinesthetic training (right panels).

Figure 11

Re-conceptualization of the visuo-spatial sketchpad as an amodal-spatial sketchpad. Modified schematic of the main modules of Baddeley's classic model of working memory including the visuo-spatial sketchpad [after Baddeley, 2003], where the added “Amodal-Spatial Sketchpad” block depicts our re-conceptualization of the visuo-spatial sketchpad as being accessible to any sensory modality.