Top Banner

Click here to load reader

Positron-emission tomography studies of cross-modality inhibition in selective attentional tasks: Closing the “mind’s eye

Jun 24, 2015


Published in 1994, this groundbreaking paper featured the research of Professor Per Roland, Professor Ryuta Kawashima (of “Brain Training” fame) and Professor Brendan O’ Sullivan.

This landmark research was the first to prove in human brain imaging studies that visual attention is impaired when we do other attention-competing tasks such as manual tasks such as using mobile phones while driving.

  • 1. Proc. Natl. Acad. Sci. USA Vol. 92, pp. 5969-5972, June 1995 NeurobiologyPositron-emission tomography studies of cross-modality inhibition in selective attentional tasks: Closing the "mind's eye" (human brain activity/regional cerebral blood flow/attention/deactivation)RYUTA KAWASHIMA, BRENDAN T. O'SULLIVAN, AND PER E. ROLAND Division of Human Brain Research, Department of Neuroscience, Karolinska Institute, S-171 77, Stockholm, SwedenCommunicated by Seymour S. Kety, National Institutes of Health, Bethesda, MD, March 14, 1995 (received for review April 20, 1994)matching (11)]. The two tasks were matched in terms of their performance difficulty and regional changes in CBF were identified by standard image subtraction techniques in which the task state is compared to a similar control state. One of the studies (tactile shape matching) was performed with the subjects' eyes open in both the task and control states so that the "eyes open" condition was matched before subtracting the images. The other somatosensory study (roughness discrimination) was performed with the eyes closed in both the task and control states, so that this condition also was matched before image subtraction. The two somatosensory tasks were chosen to specifically examine whether hypothesized decreases in rCBF in nonattended areas such as the visual cortical areas during somatosensory tasks would still occur irrespective of the general level of visual input (and blood flow values).It is a familiar experience that we tend to ABSTRACT close our eyes or divert our gaze when concentrating attention on cognitively demanding tasks. We report on the brain activity correlates of directing attention away from potentially competing visual processing and toward processing in another sensory modality. Results are reported from a series of positron-emission tomography studies of the human brain engaged in somatosensory tasks, in both "eyes open" and "eyes closed" conditions. During these tasks, there was a significant decrease in the regional cerebral blood flow in the visual cortex, which occurred irrespective of whether subjects had to close their eyes or were instructed to keep their eyes open. These task-related deactivations of the association areas belonging to the nonrelevant sensory modality were interpreted as being due to decreased metabolic activity. Previous research has clearly demonstrated selective activation of cortical regions involved in attention-demanding modalityspecific tasks; however, the other side of this story appears to be one of selective deactivation of unattended areas.MATERIALS AND METHODS Several points of methodology were critical to the performance of these studies. First, it was necessary to obtain quantitative data on absolute rCBF changes (in ml per 100 g of brain tissue per min) since normalization procedures routinely used in many other PET studies could artefactually lead to increases and reciprocal decreases in rCBF values. Absolute measures of rCBF required brachial arterial cannulation and continuous arterial sampling to define input curves after each bolus injection of the radioisotope. High-resolution functional images (full width at half maximum, 4.5 mm) were obtained by using an 8-ring (15 slice) PET camera (PC2048-15B), which has an interslice interval of 6.7 mm (12). The freely diffusible tracer [15O]butanol (13) was used in preference to H2150. Anatomical standardization and accurate functional localization was obtained by coregistration with magnetic resonance imaging (MRI)-defined anatomy by using a computerized brain atlas program (14, 15), which corrects interindividual differences in brain shape and size by both linear and nonlinear parameters in order to reformat all individual images into standard atlas anatomy. The roughness discrimination task reported here was performed with the eyes closed, while the tactile matching task was performed with the eyes open. Both tasks were performed with the right hand. In roughness discrimination, nine subjects performed a series of two alternative forced-choice discriminations of quantified roughness stimuli of known wavelength, amplitude, and stimulus energy (16) and indicated with a thumbs-up response only if the stimulus presented second was perceived as "rougher" than the first. The control state was rest with eyes closed. The tactile matching task required other subjects to match a spherical ellipsoid presented to their right hand, with one member of a linear array of similar ellipsoids hidden from view behind a white curtain in front of them. The right hand was used for all palpations, and they indicated their choice of a matching stimulus by pointing with their right indexRegional cerebral blood flow (rCBF) changes in the human brain have now been extensively studied by positron-emission tomography (PET) methods (1). Regional changes in rCBF are monotonically related to regional changes in cerebral metabolic rate, in particular the metabolic demands of maintaining the transmembrane ionic gradients of active neurons (1-4). Brain structures that actively participate in the performance of specific cognitive tasks can be identified as discrete regions of increase in rCBF. During specific cognitive tasks, our attention is selectively focused on the relevant sensory modality or submodality from which information is necessary to successfully perform the task. In behavioral terms, stimuli within the focus of attention are generally discriminated more quickly and accurately, are registered more vividly in awareness and memory, and exert greater control over behavior than do unattended stimuli (5, 6). In physiological terms, selective attention is described as changes in the excitability of cortical neurons that are limited to, or focused on, a specific sensory modality or submodality (1, 7). Increases in rCBF associated with these changes in synaptic metabolic activity can then be identified in modality-specific tasks (8, 9). Behavioral models of selective attention generally accept the notion that attention has a limited capacity, which must be flexibly distributed among competing processes (5). The question arises, therefore, what is happening neurobiologically to cortical areas of another sensory modality which is not being attended during the performance of a task? In particular, is there evidence of inhibition or deactivation in these regions which are not being attended during the performance of a cognitive task? To answer this question, we performed two PET studies in nine normal volunteers while they were engaged in somatosensory tasks [roughness discrimination (10) and tactile shape The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. 1734 solely to indicate this fact.Abbreviations: rCBF, regional cerebral blood flow; PET, positronemission tomography; MRI, magnetic resonance imaging.5969

2. 5970Neurobiology: Kawashima et al.finger. The subjects' eyes were open throughout this study and fixated on a cross drawn on the curtain in front of them. In the control state the subjects lay quietly without moving or speaking and fixated the cross with no specific task to perform. Throughout the PET measurements, the electroencephalogram and the electrooculogram were monitored continuously. The subjects' behavior was also monitored continuously with video cameras. The tests started at the start of the injection of isotope and continued for 180 sec. Subjects had their PET studies as well as MRI tomographs performed with the same bite-fixation stereotaxic helmets in order to correlate functional and anatomical data. Anatomical structures of each subject's MRI were fitted interactively using the computerized brain atlas (14, 15). All PET and MRI images were then transformed into the standard atlas brain anatomy using these parameters. The precision of the reformation process has a SD of 2-3 mm in the localization of the inner and outer brain surfaces (15). Subjects received 70 mCi ("1 mCi/kg; 1 Ci = 37 GBq) of [150]butanol as a bolus intravenous injection at the commencement of each PET run, which lasted for 80 sec. Images were reconstructed with a Hanning filter of 4 mm and were displayed with a pixel size of 2.01 x 2.01 mm. There was no further filtering of images. The arterial radiotracer concentration was measured continuously and the arterial partial pressures of 02 and CO2 (Po2 and Pco2) were measured repetitively. The rCBF was calculated by the dynamic approach on the data sampled between 0 and 80 sec after the start of the injection in frames of 5 sec each (17, 18). The rCBF images were corrected according to the arterial Pco2 measured during each PET procedure. The correction was done before test minus control subtractions to the arterial Pco2 level of the control (18). Increases in rCBF were calculated by voxel-by-voxel subtractions of the control state images from the corresponding images of each task state. Decreases in rCBF were calculated by voxel-by-voxel subtractions of the task state images from the corresponding images of each control state. All images of the brain were anatomically standardized as described above, and mean change images, variance images, and descriptive Student's t images were calculated voxel by voxel. The procedures and statistical analysis were described extensively in a recent report (18). The criterion used for accepting rCBF changes in adjacent clustered voxels as activations gives an average probability of 0.9 of finding one false-positive cluster (and 1.83 and occurring in clusters of size 12 and above; all other voxels were set to 0. This image is called a cluster image. In this image only clusters of size 12 and above having1.83 are shown and considered regions of changed rCBF. In Table 1, the cluster sizes of the activated fields are shown in cm3. One voxel had a volume of 4

Welcome message from author
This document is posted to help you gain knowledge. Please leave a comment to let me know what you think about it! Share it to your friends and learn new things together.