Saturday, February 18, 2012

That's Impossible! How the Brain Processes Impossible Objects

Relativity, by M.C. Escher.


The artwork of M.C. Escher is famous for its visual trickery. The human visual system tries to project the two dimensional image onto a three dimensional scene, but the perspective is contradictory: it cannot exist in the real world. These impossible constructions violate the laws of geometry and fascinate consumers of t-shirts, posters, and Apple products.

How does the brain represent these illusory staircases and towers? While a fascinating topic of study in the field of object perception (Levy et al., 2004), Escher prints can make for overly complicated stimuli in neuroimaging experiments. Simpler 2D figures, such as the impossible objects drawn by Swedish artist Oscar Reutersvärd, have been used in fMRI experiments (Soldan et al., 2008).



An extensive collection of 810 impossible objects is available from Impossible World, which is a fantastic resource1 maintained by Vlad Alexeev.

Previous neuroimaging experiments have used the possible/impossible object decision task to study the neural correlates of perceptual priming, an implicit form of memory. Behaviorally, repeated presentation of possible objects results in faster decision times, and this priming effect is smaller (Soldan et al., 2008) or non-existent (Schacter et al., 1995) for impossible objects. Neurally, the phenomenon of repetition suppression, or the reduction in neural activity seen upon repeated stimulus presentation, is thought to reflect facilitated perceptual processing (and perhaps behavioral priming).2 Repetition suppression predicts behavioral priming for possible objects (Habeck et al., 2006):
A set of occipital, parietal, and temporal brain regions decreased their activation across presentations, including bilateral middle occipital gyrus, left precuneus, right supramarginal gyrus, as well as some frontal and thalamic areas, such as right inferior frontal gyrus, left cingulate gyrus, and right thalamus.
However, no such relationship was observed for impossible objects.

The previous studies focused on varieties of repetition priming and whether there is a "structural description system" that facilitates the identification of perceptually coherent objects. A recently published article was specifically interested in the neural basis of impossible figures and how they are represented in the visual cortex (Wu et al., 2012). The stimuli were impossible and possible exemplars of the two-pronged trident (Fig. 1 below), shown at four different angles.


Fig. 1 (Wu et al., 2012). Examples of stimulus figures used in impossible condition and possible condition. (a) Is an impossible figure and (b) is a possible figure [that] resembles the former.

The paper started by reviewing the basic neuroanatomy of the visual system and its division into dorsal ("where") and ventral ("what") visual streams. Objects are primarily represented in the ventral stream, and the lateral occipital complex (LOC) is one area that seems to be specialized for object recognition. The authors predicted that impossible objects would be difficult for the LOC to process; therefore, additional regions would be recruited:
In the present study, we thought that the 3D structures of impossible figures might be difficult to be represented by object-selective regions (such as the LOC), and the impossible perceptions might be derived from detecting the contradiction in interpretation of the 3D structure. Therefore, we postulated that both the brain regions in the dorsal visual pathway, such as the SPC [superior parietal cortex] related to the perceptual ambiguities resolving and perceptual content modifying, and the brain areas related to the object-selective regions in the ventral pathway would be involved in the impossible figures processing.
Nineteen participants performed the possible/impossible object decision task (30 trials of each condition) while their brains were scanned. Four participants showed repetition priming in the task (first 15 trials of each condition slower than the last 15) and were excluded. The remaining subjects did not show priming.3 Personally, I would have used 30 unique possible and impossible figures to avoid priming effects entirely.

What were the results? As predicted, regions in both dorsal and ventral visual streams showed greater activation for impossible than for possible figures: right superior parietal in the former and right fusiform and inferior temporal gyri in the latter.
The right SPG in the dorsal visual pathway might be related to spatial information processing and the right LOC (FG and ITG) in the ventral visual pathway (the object-selective regions) might be related to the representation of the impossible 3D structure. Therefore, our results indicated that the impossible 3D structure might be difficult to be represented by human visual system, and the impossible perception might be derived from the detecting and resolving the contradiction in the subjects’ interpretations according to different perceptions triggered by 3D cues.

Fig. 2 (Wu et al., 2012). Brain regions showing significant difference between impossible condition and possible condition [FEW-corrected threshold of P < 0.05 at the cluster level (P < 0.001, 10 contiguous voxels cutoff at the voxel level)].

There were no brain regions that showed greater activation for possible objects.

The authors suggested that their ventral stream regions are part of LOC, although this is debatable. In the original study of Malach et al. (1995), LOC is posterior to the inferior temporal focus here, but Grill-Spector et al. (2001) state that:
...the entire region, beginning in lateral occipital cortex and extending anteriorly and ventrally into posterior temporal regions, responds more strongly to intact objects with clear shape interpretations than to control stimuli that do not depict clear shapes.
LOC doesn't seem to differentiate between familiar objects and unfamiliar objects with clear 3D interpretations (e.g. Henry Moore sculptures). At any rate, what's interesting here is that LOC was more active for impossible objects, suggesting that "the 3D spatially impossible structure could, [with difficulty], be represented by the visual system." And that, along with greater activity in the right superior parietal cortex, is how the brain processes impossible objects.


Footnotes

1 Perhaps a link to Impossible Worlds (810 figures as line drawings and grayscale images) can be added to the Tarr Lab database.

2 Interpreting neural repetition suppression effects as a reflection of behavioral priming is complicated, however (Horner & Henson, 2012).

3 However, the interaction effect approached significance (p=.083).


References

Grill-Spector K, Kourtzi Z, Kanwisher N. (2001).The lateral occipital complex and its role in object recognition. Vision Res. 41:1409-22.

Habeck C, Hilton H, Zarahn E, Brown T, Stern Y. (2006). An event-related fMRI study of the neural networks underlying repetition suppression and reaction time priming in implicit visual memory. Brain Research 1075:133-141.

Horner AJ, Henson RN. (2012). Incongruent abstract stimulus-response bindings result in response interference: FMRI and EEG evidence from visual object classification priming. J Cogn Neurosci. 24:760-73.

Levy EK, Levy DE, Goldberg ME. (2004). Art and the brain: the influence of art on Roger Shepard's studies of mental rotation. J Hist Neurosci. 13:79-90.

Malach R, Reppas JB, Benson RR, Kwong KK, Jiang H, Kennedy WA, Ledden PJ, Brady TJ, Rosen BR, Tootell RB. (1995). Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc Natl Acad Sci 92:8135-9.

Schacter DL, Reiman E, Uecker A, Polster MR, Yun LS, Cooper LA. (1995). Brain regions associated with retrieval of structurally coherent visual information. Nature 376:587-90.

Wu, X., Li, W., Zhang, M., & Qiu, J. (2012). The neural basis of impossible figures: Evidence from an fMRI study of the two-pronged trident Neuroscience Letters, 508 (1), 17-21 DOI: 10.1016/j.neulet.2011.11.064

Image by Josep V. Molins, from SOME THOUGHTS ON IMPOSSIBLE FIGURES.

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