Large, colorful, or noisy? Attribute- and modality-specific activations during retrieval of perceptual attribute knowledge

MARION L. KELLENBACH 0 MATTHEW BRETT 0 KARALYN PATTERSON MRC Cognition 0 Brain Sciences Unit 0 Cambridge 0 England 0 0 KELLENBACH, BRETT, AND PATTERSON Position emission tomography was used to investigate whether retrieval of perceptual knowledge from long-term memory activates unique cortical regions associated with the modality and/or attribute type retrieved. Knowledge about the typical color, size, and sound of common objects and animals was probed, in response to written words naming the objects. Relative to a nonsemantic control task, all the attribute judgments activated similar left temporal and frontal regions. Visual (color, size) knowledge selectivelyactivated the right posterior inferior temporal (PIT) cortex, whereas sound judgments elicited selective activation in the left posterior superior temporal gyrus and the adjacent parietal cortex. All of the attribute judgments activated a left PIT region, but color retrieval generated more activation in this area. Size judgments activated the right medial parietal cortex. These results indicate that the retrieval of perceptual semantic information activates not only a general semantic network, but also cortical areas specialized for the modality and attribute type of the knowledge retrieved. - Stored knowledge about object concepts is generally described as comprising both functional/associative information, such as what an object is used for and where it is found, and perceptual/sensory information, such as what the object looks like (e.g., color, size, shape), any sound it makes, its smell, taste, and texture, and so on. It has been further proposed that the cortical regions subserving different aspects of semantic representations might be located in or near the sensory or motor cortices through which the knowledge is acquired and experienced (e.g., Allport, 1985; Gainotti, Silveri, Daniele, & Giustoli, 1995; Pulvermller, 1999). Although direct evidence for the contribution of separable neural systems to the representation and processing of different types of perceptual knowledge has been provided by a small number of neuropsychological studies, attempts to localize perceptual attribute knowledge by using neuroimaging techniques either have been restricted to a single type of visual attribute (color) or have examined a range of broadly defined visual attributes (e.g., [relative] size/ shape judgments, feature/part identification). If the re We thank both the staff at the Wolfson Brain Imaging Centre, particularly Nahal Mavaddat, Iona Kendall, Tim Donovan, Dylan Pritchard, and Gary Hawes, and the volunteers who underwent the scans. We are also grateful to Dr. Facundo Manes for defining the temporal lobe region of interest for us. Correspondence concerning this article should be addressed to M. L. Kellenbach, MRC Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge CB2 2EF, England (e-mail: marion. ). trieval of different perceptual attributes engages nonidentical and sensorily relevant cortical regions, careful definition of the attribute(s) of interest and comparison across a variety of attributes is critical. The position emission tomography (PET) study reported here was designed to investigate the distinctiveness of the neural substrates involved in various types of perceptual attribute knowledge, both within and between modalities. Neuropsychological Data Few neuropsychological studies have reported selective impairment or sparing of the knowledge of various perceptual attributes, and the insights provided by even these few studies are limited by a lack of systematicity in the range of attributes tested. Localization of the critical underlying neural structures has also been problematic, because most reported cases involve extensive and /or diffuse cortical damage. Nonetheless, the specific perceptual attribute dissociations reported in those few studies that have investigated a range of relevant attributes provide some support for fractionation of perceptual semantic attributes and their separate cortical localizations. Several studies have reported the relative sparing of knowledge pertaining to the perceptual attribute of size, in the context of impaired knowledge about other visual perceptual attributes (e.g., the color, overall shape, and parts of objects; Coltheart et al., 1998; Forde, Francis, Riddoch, Rumiati, & Humphreys, 1997; Sartori & Job, 1988; see also Sheridan & Humphreys, 1993). This dissociation has led to suggestions that size information may be a nonperceptual semantic attribute, rather than a visual perceptual attribute (Sartori & Job, 1988; see also Coltheart et al., 1998), or may represent a higher level of visual representation that may be spared when more specific knowledge is impaired (Sartori & Job, 1988). Alternatively, size knowledge can be viewed as distinct from other visual object properties in that it is more spatially defined. In the absence of clear empirical evidence favoring any of these alternatives, the present study takes the last possibility as the working hypothesis to be investigated. To our knowledge, no patient has yet been reported with a selective impairment of size knowledge relative to other visual attributes. Of course, not all perceptual attributes are visual, and two neuropsychological studies have shown that auditory information may be spared in patients with impaired knowledge about visual attributes (excluding size; Coltheart et al., 1998; Sartori & Job, 1988). A selective impairment of auditory relative to visual knowledge has not yet been reported. Although extremely limited, these neuropsychological data suggest that the visual attribute of color may be dissociable from both size (another visual attribute) and sound knowledge and provide support for the general proposal that knowledge about the perceptual attributes of objects involves a cortical network comprising functionally and neuroanatomically distinct regions. Neuroimaging Data Functional imaging has enabled investigation of the neural regions associated with different types of semantic knowledge in normal subjects. Only four neuroimaging studies to date, however, have directly compared the retrieval of nonperceptual and (visual) perceptual knowledge (Cappa, Perani, Schnur, Tettamanti, & Fazio, 1998; Martin, Haxby, Lalonde, Wiggs, & Ungerleider, 1995; Mummery, Patterson, Hodges, & Price, 1998; ThompsonSchill, Aguirre, DEsposito, & Farah, 1999). Although all four studies have reported increased activation in the temporal lobe (as well as a number of frontal and parietal regions) for visual perceptual knowledge, relative to functional attributes and nonsemantic control tasks, various regions of the temporal lobe were implicated. Both the Cappa et al. and the Thompson-Schill et al. studies reported activation of (somewhat different) regions of the left or bilateral posterior inferior temporal (PIT) cortex, but Mummery et al. (1998) found that the left the anteromedial temporal co (...truncated)