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Behavioral Change and Its Neural Correlates in Visual Agnosia After Expertise Training

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Behavioral Change and Its Neural Correlates in Visual Agnosia After Expertise Training Behavioral Change and Its Neural Correlates in Visual Agnosia After Expertise Training Marlene Behrmann1, Jonathan Marotta2, Isabel Gauthier3, Michael J. Tarr4, and Thomas J. McKeeff 5 Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/17/4/554/1757207/0898929053467613.pdf by guest on 18 May 2021 Abstract & Agnosia, the impairment in object and face recognition S.M. showed significant improvement in recognizing Greebles, despite intact vision and intelligence, is one of the most although he did not attain normal levels of performance. He intriguing and debilitating neuropsychological deficits. The was also able to recognize untrained Greebles and showed goal of this study was to determine whether S.M., an individual improvement in recognizing common objects. Surprisingly, his with longstanding visual agnosia and concomitant prosopag- performance on face recognition, albeit poor initially, was nosia, can be retrained to perform visual object recognition even more impaired following training. A comparison of pre- and, if so, what neural substrates mediate this reacquisition. and postintervention functional neuroimaging data mirrored Additionally, of interest is the extent to which training on one the behavioral findings: Face-selective voxels in the fusiform type of visual stimulus generalizes to other visual stimuli, as gyrus prior to training were no longer so and were, in fact, this informs our understanding of the organization of ventral more Greeble-selective. The findings indicate potential for visual cortex. Greebles were chosen as the stimuli for experience-dependent dynamic reorganization in agnosia with retraining given that, in neurologically normal individuals, the possibility that residual neural tissue, with limited capacity, these stimuli can engage the fusiform face area. Posttraining, will compete for representations. & INTRODUCTION the second involves the cortical substrate that might Visual agnosia refers to the well-known neuropsycho- mediate this reacquisition. logical deficit in which recognition of visual stimuli is impaired despite intact vision and preserved semantic knowledge and intelligence (Farah, 2004). Although Experience-dependent Change in the severity of agnosia varies, so does the nature of Neuropsychological Deficits the impairment; some individuals are impaired at recog- Whether experience-dependent change in visual agnosia nizing objects as well as faces whereas others may be is at all possible is of considerable interest in light of impaired at, for example, object and word recognition recent studies showing substantial compensation and with relatively preserved face recognition. Exactly why recovery along with dynamic reorganization in damaged thesepatternsofco-occurrenceemergeisamatter adult cortex (Kolb, Gibb, & Robinson, 2003; Pizzamiglio, of ongoing debate (Riddoch & Humphreys, 2003; Bux- Galati, & Committeri, 2001). For example, several studies baum, Glosser, & Coslett, 1999; Humphreys & Rumiati, document the recruitment of alternative neural tissue 1998; Rumiati & Humphreys, 1997; Rumiati, Humphreys, during the course of recovery from aphasia (Riecker, Riddoch, & Bateman, 1994; Farah, 1991, 1992, 1999). In Wildgruber, Grodd, & Ackermann, 2002) via activa- addition to this debate, many other outstanding issues tion of perilesional tissue in the lesioned hemisphere remain in the study of agnosia. One such issue, which (Warburton, Price, Swinburn, & Wise, 1999; Small, Flores, is the focus of this article and which has received sur- & Knoll, 1998), via recruitment of homologous tissue prisingly little scientific attention, is whether agnosic in the opposite hemisphere (Thulborn, Carpenter, & individuals can be retrained to perform visual recogni- Just, 1999; Small et al., 1998), or both (Rosen et al., tion. If such retraining is possible, 2 other immediate 2000). Similarly, many studies have documented plastic- questions come to mind: The first concerns the extent ity of motor circuits in adults with hemiparetic stroke, and nature of the generalization from the training and providing support for a compensatory role of preex- isting uncrossed motor neural pathways (Pizzamiglio et al., 2001). 1Carnegie Mellon University, 2University of Manitoba, 3Vander- Functional reorganization has also been noted in bilt University, 4Brown University, 5Princeton University visual cortex in adults. For example, increased activation D 2005 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 17:4, pp. 554–568 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929053467613 by guest on 24 September 2021 is observed in the visual cortex in blind individuals electrophysiological and functional imaging studies, doc- (Elbert & Rockstroh, 2004), and learning-dependent umenting a face-specific response in particular regions of changes in the corresponding retinotopic area of visual the ventral cortex of the brain (Tsao, Freiwald, Knutsen, cortex are noted in normal observers following intensive Mandeville, & Tootell, 2003; Bentin & Deouell, 2000; monocular training on visual texture discrimination Kanwisher, 2000; Kanwisher, McDermott, & Chun, 1997; (Schwartz, Maquet, & Frith, 2002). Of particular rele- McCarthy, Puce, Gore, & Allison, 1997; Sergent, Ohta, & vance are studies documenting behavioral and neural MacDonald, 1992). An alternative conceptualization is changes in individuals with lesions in visual cortex; there that the ventral visual system is organized in a more are several studies documenting a strong positive rela- distributed fashion with many different regions partici- tionship between the recovery of visual function and pating (perhaps to a greater or lesser extent) in the Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/17/4/554/1757207/0898929053467613.pdf by guest on 18 May 2021 improved metabolism of striate cortex (Pleger et al., recognition of all visual stimuli (Pietrini et al., 2004; 2003; Braus, Hirsch, Hennerici, Henn, & Gass, 1999; Haxby et al., 2001; Ishai, Ungerleider, Martin, Schouten, Bosley et al., 1987), attesting to the efficacy of interven- & Haxby, 1999). tion procedures. The controversy between a domain-specific organiza- These findings suggest that dynamic cortical reorga- tion of visual classes versus a more generic system has nization is possible in the human adult cortex. Few not been resolved and the reader is referred to recent studies, however, are specifically devoted to tracking articles for further explication (Grill-Spector, Knouf, & the effects of rehabilitation on agnosia and the associ- Kanwisher, 2004; Grill-Spector, 2003; Tarr & Cheng, ated cortical plasticity (Burns, 2004; Seniow, Polanowska, 2003; Maurer, Le Grand, & Mondloch, 2002; Haxby Mandat, & Laudanski, 2003). Of the studies that have et al., 2001; Kanwisher, 2000; Tarr & Gauthier, 2000). tracked recovery of individuals with agnosia, minimal, if In this article, we implement category-specific retraining any, change in the behavioral performance is reported. in an individual with object agnosia and prosopagnosia For example, Caldara et al. (submitted) reported the using one class of stimuli and then examine the extent failure of a patient with a face recognition impairment to which there is generalization to other classes of stim- (and preserved object recognition) to acquire expertise uli. If different classes of objects are represented inde- with visual input. Furthermore, in those few cases where pendently, perhaps by discrete modules, then one might change has been reported, it remains unclear whether not expect a trained class of stimuli to have any influ- the change is attributable to the adoption of compen- ence on a second, untrained class. In contrast, if re- satory strategies or to the amelioration of the object training in one class has consequences for performance recognition deficit per se (Thomas, Forde, Humphreys, on a second class, this might implicate more general & Graham, 2002). A primary goal of this study, then, visual recognition mechanisms. is to examine the psychological and neural bases of The training regimen we adopt involves the use of experience-dependent change following focused inter- Greebles and has been previously shown to increase vention in an adult with longstanding visual agnosia and visual expertise in nonneurological individuals. In these accompanying prosopagnosia. studies (Gauthier, Williams, Tarr, & Tanaka, 1998; Gauthier & Tarr, 1997, 2002), participants are trained to identify individual Greebles, novel 3-D-rendered objects made of a vertically oriented ‘‘body’’ with 4 pro- Implications of Retraining for Organization of the truding appendages and sharing the same basic ele- Ventral Visual Cortex mental features in a canonical configuration with other Although the outcome of a study on recovery from members of the class (see Figure 1). The claim is that, as visual agnosia is informative from a clinical point of is true for faces, local shape and surface features may not view, such an intervention study can also increase our suffice for the purpose of discrimination and identifica- understanding of the organization of the cortical visual tion of individual Greebles given their perceptual simi- system. One issue that is currently debated in cogni- larity. To efficiently differentiate individual exemplars of tive neuroscience concerns the organization of the faces or Greebles, additional details and ‘‘configural’’ ventral temporal visual system. Some researchers have or relational information
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