Proc. Nati. Acad. Sci. USA Vol. 91, pp. 9965-9969, October 1994 Neurobiology Visual form discrimination from color or motion cues: Functional anatomy by positron emission tomography (regional cerebral blood flow/human visual cortex/form) B. GULYAS*t, C. A. HEYWOODt, D. A. POPPLEWELL*, P. E. ROLAND*, AND A. COWEYt *Laboratory for Brain Research and Positron Emission Tomography, Department of Neuroscience, Karolinska Institute, S-171 77 Stockholm, Sweden; and tDepartment of Experimental Psychology, Oxford University, South Parks Road, Oxford, OX1 3UD, United Kingdom Communicated by James M. Sprague, June 29, 1994 (receivedfor review February 8, 1994) ABSTRACT To explore the extent to which various corti- mans using various visual form-related psychophysical par- cal functional pathways are Involved In processing and ana- adigms have shown a large number of cortical regions to be lyzing different types of information that yield the same active during the different form tasks (20-24). perceptual entity, we mapped anatomical structures in the With the intention of exploring in the human visual system human brain participating in the dimination ofvisual forms (i) whether motion and color are analyzed by identical, mediated either by motion or color cues. Changes in regional overlapping, or different cortical substrata and (ii) whether cerebral blood flow were measured in 10 young male volunteers discrimination of visual form mediated by motion and color with positron emission tomography and with [15O1butanol. cues engage the same cortical regions, we measured regional During the measurements, the subjects performed four visual cerebral blood flow (rCBF), as an indicator of regional discrimination tasks (form-from-motion, motion alone, form- cerebral metabolism, with PET, using [150]butanol as tracer, from-color, and color alone discrimination). The individual in 10 healthy male volunteers while they performed a series regional cerebral blood flow images were standardized in shape of visual discrimination tasks. and size with the help of a computerized brain atlas. Subtrac- tion Images were determined and averaged across data from all subjects. The resulting images were analyzed for statistically METHODS signiicant changes between specific and reference tasks. The Subjects. Ten healthy male volunteers (age, 28.2 ± 2.7 discimiation of form by means of motion cues activated years, mean ± SD) participated. They were fully informed functional fields bilaterally in the inferior and lateral occipital about the objectives, details, and risks ofthe experiment and gyri, in the lingual, anterior iate, middle frontal and gave a written consent, in agreement with the Helsinki orbitofrontal gyri, and in the left fusiform and right inferior Declaration and the Code of Federal Regulations: Protection temporal gyri. Form discrimination by color cues resulted in of Human Subjects (25, 26). The study was approved by the activation bilaterally in the inferior temporal, lateral occipital, Ethical and Radiation Safety Committees of the Karolinska and orbitofrontal gyri, the left precuneus and intraparletal Hospital. Nine subjects were right handed and one subject sulcus, and the right precentral gyrus. The regions engaged in was left handed, as assessed the the two kinds of form discrimination did not overlap, demon- by Edinburgh handedness strating that differences in visual forms mediated by color or inventory (27). Seven subjects were emmetropes, and three motion cues are processed and analyzed by disparate networks had appropriate spectacle correction. The subjects' color of functional fields in human cerebral cortex. vision was tested before the experiment using a Velhagen chart (28). None of them had any manifest or hidden color vision or visual field deficit. Several physiological observations suggest that neuronal Four PET measurements were taken on the subjects while signals about color and motion are processed and analyzed by visual different functional pathways at early levels in the primate they performed discrimination tasks. The tasks were visual system (1-7). Although there are interactions between interleaved in different orders in different subjects. During the systems coding color and motion (8-10), they and their the scan, the subjects were comfortably placed in supine underlying pathways are regarded as initially independent position on the camera bed. With the exception of the (11, 12). Both the color and motion systems provide signals ambient noise of the scanners, the electroencephalogram that can elicit the same categories ofvisual perceptual entity, (EEG) apparatus, and the arterial pump, there was no noise such as contour or form. in the room, which was kept at 230C. The auditory environ- In monkeys, several studies show that cells sensitive to ment was not disturbed by any movements or speech by the visual form are located in cortical regions along a "ventral" personnel who were in a remote control room. The subjects occipitotemporal visual pathway and it has often been were required not to move or activate their muscles, to say claimed that the detailed analysis of visual forms occurs, in anything, or to change the respiratory rhythms after the great part, in the inferior temporal cortex (13-17). It has also infection, with the exception of pressing a response key to been shown that there are form-selective neurons in the register their responses with their right middle or index macaque inferior temporal cortex that are equally activated fingers. The visual field of the subjects, including the pro- by visual forms formed by luminance, motion, or texture cues jection screen, was isolated from the rest ofthe room by black (18). However, claims that there is a center or are centers in drapes. the brain [the "form area(s)"] exclusively specialized for the Visual Stimulation. The stimulus displays were presented perception of complex forms, such as faces, have recently on a 20-inch color monitor [Microvitec 2038 with a screen been challenged by lesion studies in monkeys (19). Further- more, positron emission tomography (PET) studies in hu- Abbreviations: PET, positron emission tomography; rCBF, regional cerebral blood flow; gCBF, global cerebral blood flow; EEG, elec- troencephalogram; MR, magnetic resonance; PaCO2, arterial partial The publication costs ofthis article were defrayed in part by page charge CO2 pressure; PaO2, arterial partial 02 pressure; CBA, computerized payment. This article must therefore be hereby marked "advertisement" brain atlas. in accordance with 18 U.S.C. §1734 solely to indicate this fact. tTo whom reprint requests should be addressed. 9965 Downloaded by guest on September 28, 2021 9966 Neurobiology: Gulyds et al. Proc. Natl. Acad. Sci. USA 91 (1994) resolution of 768 x 576 pixels and a viewing distance of 125 task, squares and rectangles were defined by the coherent cm (10 = 2.2 cm; 1 inch = 2.54 cm)]. The screen subtended motion of all their constituent pixels and the form discrimi- 180 x 160. For each task a horizontal row of three stimuli, nation was identical in other respects to the form-from-color separated by 30, was presented on the screen against a discrimination. stationary background composed of a yellow [CIE (Commis- Brain Scanning. A high-resolution nuclear magnetic reso- sion International d'tclairage) coordinates: X = 0.510; Y = nance (MR) scan (GE 3514 MR camera, 1.5 Tesla) was made 0.426] 10%1 random pixel pattern. The luminance of the pixels ofeach brain (both proton-enhanced and T2-weighted images: was 10.0 cd/M2. Form-from-motion and form-from-color spatial resolution, 0.5 mm; slice thickness, 4 mm; interslice discriminations were each paired with their reference tasks, distance, 6.5 mm; spin echo, TR = 2300 msec and TE = 25 motion discrimination and color discrimination, respectively. msec and 90 msec). The head fixations in the MR and PET For image analysis, the images revealed by the reference task scans were identical (29, 30) so that the corresponding MR were subtracted from those revealed by the corresponding and PET images were superimposable. The PET scanning [15 discrimination task. transaxial slices at 6.5 mm (distance)] was made by a Scan- The subject had to indicate the odd-one-out, which ap- ditronix PC2048-15B positron emission tomograph, having a peared either to the right or left of the row of stimuli, by 5-mm in-plane spatial resolution (31, 32). [150]Butanol, a pressing one of two buttons. There was no time pressure on freely diffusible flow tracer, was used to measure rCBF (33). the subject and a new trial immediately followed a response. During the experiments EEG, electrooculogram (saccadic The difficulty of the discrimination was varied from trial to eye movements of an amplitude >1 degree), arterial ra- trial. Three consecutive correct responses resulted in a more diotracer concentrations, arterial partial 02 pressure (PaO2) difficult discrimination. An easier discrimination followed a and arterial partial CO2 pressure (PaCO2) levels were con- single error. Predetermined thresholds for each discrimina- tinuously monitored. The response latencies and perfor- tion ensured that the subject's performance during PET mance levels were calculated on-line. rCBF and global ce- measurements tracked his threshold. rebral blood flow (gCBF) measurements were taken during In the color discrimination task (Fig. 1), the stimuli were the tasks. Differences in rCBF between the tasks resulting three squares (2.50 x 2.50) composed of the same random dot from differences in PaCO2 were corrected (34). Other aspects pattern as the background. The red and green guns were of the method, including the adequacy of resolution param- modulated, while maintaining isoluminance, to define the eters to the were as described or vice versa. The hue present study, (35). three squares, two red and one green, Image Analysis. The MR and PET images were transferred difference was titrated by halving or doubling the depth of into the brain atlas ofBohm and Greitz modulation of the guns, with 'y correction, after correct or computerized (CBA) For the form-from-color (36, 37) and transformed into standard size and shape.