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Re-conceptualization of the visuo-spatial sketchpad as an amodal-spatial sketchpad. The spatiotopic organization and inherently parallel processing of the largest cortical map, V1, and most importantly, the small receptive fields providing the high-spatial resolution of the V1 map e. The data described in this chapter provide a direct evidence supporting such an implementation of a spatial sketchpad in human V1. It is important to note, however, that such an interpretation does not mean that V1 is em ployed for long-term storage of the memory trace, but merely for its operational activation in working memory to meet the task demands.

Moreover, in contrast to the usual format of a baseline condition, we instructed and practiced the subjects to eliminate any rehearsal of either the just-explored templates or of any other memory images for the full 20 s duration of each null interval, which was also too long to account for the known retention time of any visual or iconic image of the memory trace, which is of the order of a second or less Sperling, ; Di Lollo, ; Loftus et al.

Since the drawings were not experienced as spatial images during the null interval, they were evidently held in some other, non-conscious storage location until it was needed for the subsequent drawing task. The current analysis was not designed to directly answer the question of the role of the extrastriate suppression Fig.

This fact eliminates potential sensory mechanisms, such as a direct drive of the primary visual cortex through direct connec tions from the primary somatosensory cortex. Why is this suppression needed? We suggested that such suppression of the less relevant information that of the ground makes strong computational sense. Such an interpretation is also consistent with theoretical predictions in Tsotsos et al.

It seems logical that a similar principle of active suppression of task-irrelevant regions i. Thus, the extrastriate suppression surrounding V1 prevents any potential propagation of the entirely non-visual V1 signal through the visual hierarchy pathway, which would be an inappropriate pathway in this case.

A congenitally blind novice with no experience with drawing or writing provides an ideal paradigm for investigating the earliest stages of V1 reorganization, and also provides for a critical probe of our amodal sketchpad idea, because congenital blindness eliminates the possibility of any visual mechanisms influencing the neural processing. Specifically, it abolishes not only the bottom-up visual input but also any potential top-down visual processing, such as visual imagery since congenital blindness eliminates any visual experience on which to base such processing.

We were lucky to find such an absolute novice. This individual was well-adapted to operating in the spatial world, including longstanding familiarity with complex tactile manipulations and Braille reading, but had no drawing, writing or even pen-holding experience. Functional MRI was run before and after a week of Cognitive-Kinesthetic training in order to test our hypothesis that V1 uses an amodal spatial representation in its operation as the putative memory buffer, and to investigate the temporal evolution of brain reorganization as a function of learning to draw.

The congenitally blind subject was a year-old right-handed female, totally blind with no light perception, who lost her vision shortly after birth as a result of rubella German measles in her expectant mother, severely and permanently damaging the fetal optic nerves, and also degrading her hearing to some degree. She had not been previously studied by fMRI or behavioral methods of any kind.

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She is a sophisticated intellect and a fluent Braille reader, with a graduate education and lifetime employment including the professional use of a computer keyboard, and was highly motivated to participate in the study. Nevertheless, despite her Braille fluency, the subject had no experience with writing or drawing, so her training to draw had to start with the basics, such as the proper holding of the pen and key spatial concepts of the representation of 3D structure on a 2D plane.

She had relied heavily on active tactile exploration for her whole life, so it was quite surprising that she did not have clear idea of elementary geometric concepts such as a straight line vs a curve, right angles, etc. These issues were manifested at all levels of the experimental process — the tactile recognition and memorization phase, the memory recall in drawing, the understanding of spatial relationships, and even the kinesthetic feedback and self-evaluation of her own performance.

For example, she could think she had just drawn a straight line when she had actually drawn an almost-closed curve, and so on. Another advantage was the fact that this subject was an intelligent adult, able both to readily follow instructions and to express back her introspections. The novel Cognitive-Kinesthetic technique allowed our subject to learn to draw freehand, i.

As specified in 3. The training procedure was able to inspire and motivate this blind subject to acquire the exciting drawing skill. After only a week, she significantly advanced relative to her starting level, although her capability was still not satisfactory to her. To study the dynamics of the learning process, we ran fMRI before training, as well as after a prolonged consolidation period. The focus of the analysis presented here is the occipital region along the calcarine sulcus corresponding to the location of the primary visual cortex, area V1.

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Comparison of the voxelwise parametric maps in the primary visual cortex during the MemoryDraw task reveals dramatic enhancement of the activation orange coloration in V1 green outline from negligible patchy activation before training Fig. Remarkably, the extension of post-training activation in V1 approximately corresponds to the spatial extent of that in the blindfolded normally-sighted subjects in Section 3.

Lack of task-specificity before training, but development of MemoryDraw dominance after training. Bar-graphs for the estimated activation in V1 in each hemisphere before training Fig. In contrast, after training Fig. This analysis implies a significant reorganization in the V1 response pattern as a result of training. Importantly, the V1 response in the memory-guided drawing task MD was substantially increased, while the response of the non-memory motor-control task S became insignificant.

Note that, in contrast, no such increase was present in the area of the left motor cortex controlling the drawing right hand , which even showed a reduction in response after training, as may be expected when a motor task becomes familiar e. Bar-graphs in Fig. Time-courses show the average time courses of BOLD activity black lines for the sequence of three task intervals white bars.

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Top row A, B in Fig. The advantage of training a total novice was also manifested by allowing us to capture the very early stages of functional reorganization as expressed in the changes of the time course of the BOLD responses. As seen in Fig. The pre-training response waveforms are rudimentary, poorly-developed and noisy, with a prominent transient nature and early offsets long before the end of the 20 s task periods, in spite of the continuous hand movements during the full task period these continuous hand movements are evident from both the motion-capture records and also from the fully-fledged time course in the motor hand area, Fig.

Such early offset in V1 implies that the neural response was essentially a brief transient pulse that was immediately withdrawn, suggesting an unsuccessful attempt to activate this area. The subject self-report and drawing performance were consistent with such undeveloped utilization. After training, the undeveloped pre-training waveforms undergo a total transformation into well-developed BOLD response waveforms Fig.

Notably, as a result of training, the temporal waveform of the V1 response regularized to become a good match to the linear model prediction colored curves in Fig. We no longer see the transient early-offset signals. Importantly, however, Scribble , which has no memory involvement, is lacking any significant V1 response.

This study is the first to investigate the temporal evolution of functional reorganization of V1 as a result of a non-visual memory training task. Working with an adult who was an absolute novice has the advantage that such a subject can provide full introspection and produce complex behavioral measures as opposed to working with difficult-to-communicate-with infants. This investigation thus opens a window on research in the developmental evolution of both neural and behavioral changes, capitalizing on the effectiveness of the Cognitive-Kinesthetic training to speed up the process.

Except for her blindness and reduced hearing, this congenitally blind subject was in a very good physical and mental health, with robust BOLD responses in right-hand motor cortex, M1 Fig. Thus, a primary explanation of her V1 response patterns of undifferentiated, transient activation across all the tasks Fig. The immature, early-offset waveforms suggest a rudimentary and unsuccessful attempt to activate V1, showing that, remarkably, the six decades of reliance on tactile perception in everyday tasks was evidently insufficient for the development of V1 functionality as demanded by the challenging memory-drawing task.

The rapid, learning-based recruitment of V1 in the MemoryDraw task after blind training Fig. Importantly, the use of the training paradigm itself provides causal inferences about the cross-modal changes in V1. Although a mature adult, this congenitally blind individual showed rapid functional reorganization of her brain in the process of learning to draw. It seems particularly surprising to find such reorganization in the primary visual cortex, whose main role is considered to be the early processing modality-specific information from visual input.

Thus, the drawing task was sufficiently demanding to activate functional reorganization that was not instigated by any other task during her life despite the intensive use of other forms of detailed spatial information such as Braille characters for reading. Further studies are needed to investigate the specific cross-modal mechanisms mediating the V1 reorganization; in general, there is a wide range of theoretical possibilities, such as unmasking of pre-existing connections, synaptic weight changes, or a combination of a number of different mechanisms e.

Such multidimensional consistency between the congenitally blind and the blindfolded responses is likely not to be accidental but to reflect common mechanisms operating under both short-and long-term visual deprivation. To further explore this finding, a comparative analysis of groups of congenitally and late blind individuals is described in the next section.

The eccentricity overlap of the post-training MD activation in V1 for the congenitally blind Fig. Therefore, the consistent extent of V1 activation raises a number of fundamental questions, as it is suggestive of i preservation of a form of topographic organization in V1 despite complete visual deprivation, and ii utilization of this topography by cross-modal memory. Does such a topographic operation of the amodal memory sketchpad reflect a universal i. This section does not aim to provide complete answers but to raise questions and show their legitimacy based on our results in two additional groups of totally blind people.

A group of 6 congenitally blind and 7 late-onset blind individuals were studied before and after Cognitive-Kinesthetic training. All methods were as described in the General Methods section, with delineation of the normal retinotopic and functional organization in the whole-brain averaging by means of the novel method we have developed. The late-onset blind group had blindness onsets ranging from 3 to 39 years of age.

Only patients with total ocular but not cerebral blindness, were included. Human vision is well-established to be close to adult level by the age of 3, so the primary requirements for visually processing would have been well developed before the onset of blindness in this late-onset group. Consistent with the findings from sections 3 and 4, MemoryDraw strongly activated V1 along the calcarine in both blind groups, and remarkably, the activation did not fill in the whole of V1 but extended only about half way posteriorly, covering what in the sighted would be approximately the central 10 deg retinotopic representation.

The dashed white lines in Fig. Both the late-onset blind Fig. The fact that eccentricity-robust activation was systematically obtained in V1 as a result of training in all visually-deprived populations is indicative of topographically organized non-visual processing in this earliest visual area. This paradoxical result raises an array of questions. Does retinotopy develop by a nature or nurture mechanism, or by an interplay between the two?

How would a topographic organization develop in the congenitally blind despite the absence of visual experience to drive it?

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Is its development determined entirely genetically and independently from visual stimulation in congenital blindness? How is an already developed retinotopy preserved after the total loss of visual input, as in the case of the late-onset blind subjects? How is a still functioning retinotopy, such as in the blindfolded, rapidly recruited by cross-modal memory?

What is the frame of reference for such topographic metrics? The current studies leave open questions for future research, although a basis for some answers is already emerging. Interestingly, a recent 7-T high-resolution structural MRI study in congenitally blind individuals has established the presence of another organizational landmark of V1 — the stria of Gennari — in this population Trampel et al.

This finding indicates that neither the development nor the preservation of this V1 landmark depends on the presence of visual input.

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Moreover, Cang et al. The same group has also shown, however, strong experience-based V1 plasticity in non-human experiments reviewed in Espinosa and Stryker, Thus, the plasticity mechanisms in V1 appear to be a complex interplay between genetic and environmental factors, which further tune-up and refine the rough genetically-determined layout for a recent review see Maya-Vetencourt and Origlia, Group data in the blind. A The post-training group activation in V1 for the MemoryDraw task in the late-onset blind group expanded to approximately 10 deg eccentricity dashed white line , similarly to the results in previous sections.

B Remarkably, even the group data of congenitally blind individuals with no visual experience throughout their life manifested similar eccentricity dashed white line. Detailed discussions are included in each of the experimental sections. Here, to sum up, the analyses of the fMRI data from our novel drawing-based memory paradigm and the Cognitive-Kinesthetic training led us to discover a unique pattern of V1 response, cut-off from propagation throughout the visual hierarchy by surrounding deactivation.

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Consideration of these results, in turn, excludes the most expected hypotheses and suggests a novel straightforward interpretation: That V1 in human implements the visuo-spatial working memory sketchpad concept but does so in an amodal form that transcends the sensory-modality specialization of the visual hierarchy. Based on this reasoning, we generated the prediction that, under the same memory paradigm, V1 will be activated even in the congenitally blind, who had never had any visual stimulation.

This prediction was tested in a subsequent experiment, which replicated the freehand memory-drawing paradigm in a congenitally-blind novice. The data from this unique case study confirmed our initial interpretations of i an amodal working memory role of V1, and ii a spatiotopic character of the amodal memory representation. Furthermore, they also revealed for the first time the temporal evolution of the BOLD response during this learning-based cross-modal reorganization in the primary visual cortex.


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