Hierarchical versus parallel processing in tactile object recognition: a behavioural-neuroanatomical study of aperceptive tactile agnosia.

ABSTRACT

The organization of the normal perceptual processing subserving tactile object recognition is poorly understood. While perceptual deficits associated with cases of tactile agnosia may pinpoint sites of critical interference with normal tactile information processing, the precise character of such deficits remains unclear. The aim of the present study was to explore the behavioural and neuroanatomical correlates of perceptual disturbances in two cases of unilateral aperceptive tactile agnosia. Perception of microgeometrical and macrogeometrical features was tested using an alternative forced choice paradigm. While both patients were impaired in the assessment of microgeometrical properties of objects (i.e. detecting subtle differences in grating profiles), one patient showed an additional deficit in the perception of macrogeometrical properties of objects (i.e. detecting differences in length of cuboids). The pattern of perceptual deficits for both patients suggested a severely compromised (if not totally lost) ability to recognize everyday objects. Perceptual performance improved when the patients had complementary tactile information (i.e. for intramodal comparison), despite a persistent inability to explicitly name the objects. That is, the patients were able to recognize objects, but only implicitly. Improved perceptual performance was also observed when complementary visual information was available (i.e. transmodal information transfer). In this case, the perceptual improvement was accompanied by a corresponding improvement in explicit object recognition. High resolution MRIs identified lesions in the postcentral gyrus in both patients, and additionally in the secondary somatosensory area (SII) and the posterior parietal cortex in the more severely affected patient. The results demonstrate that the underlying failure in tactile agnosia is mainly impaired perception of microgeometrical properties of objects due to a lesion of primary sensory cortex. The related neuroanatomical findings suggest a degradation of serial information processing within postcentral gyrus. In one case tactile agnosia was almost complete due to additionally impaired perception of macrogeometrical properties of objects, which correlated with the extension of lesion to the posterior parietal cortex. Importantly, the findings indicate traces of two distributed networks for tactile information processing and the associated parallel processing of complementary micro- and macrogeometrical information within postcentral gyrus and posterior parietal lobe.