Two modulatory effects of attention that mediate object categorization in human cortex

Science

Volumn 275, Issue 5301, 1997, Pages 835-838

  Rees, Geraint ^a   Frackowiak, Richard ^a   Frith, Chris ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ATTENTION; BRAIN CORTEX; CEREBELLUM; NEUROMODULATION; PREMOTOR CORTEX; PRIORITY JOURNAL; REGULATORY MECHANISM; VISUAL STIMULATION;

ADULT; AGED; ATTENTION; BRAIN MAPPING; CEREBELLUM; CEREBRAL CORTEX; FRONTAL LOBE; HUMANS; MALE; MIDDLE AGED; MOTOR CORTEX; NEURONS; REGIONAL BLOOD FLOW; TEMPORAL LOBE; TOMOGRAPHY, EMISSION-COMPUTED; VISUAL PERCEPTION;

EID: 0031024562     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.275.5301.835     Document Type: Article

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24. All participants were right-handed males aged 31 to 76 (mean 40.5 years) who gave their informed consent for participation in this study. Isoluminant ellipses subtending ∼7° of visual angle were presented at regular intervals (30, 50, 70, and 90 ellipses per minute) for 500 ms at fixation on a computer monitor ∼57 cm from the participant. The ellipses could differ in color (red, green, or blue) and orientation (horizontal or vertical). A participant indicated a categorization choice of target or nontarget by pressing a button with either the right or left index finger. A response was required for every ellipse presented. The proportion of targets was kept constant across conditions at 50%; in all other respects the stimuli and presentation were identical in all conditions. The assignment of fingers was made before the scanning session and was the same for all scans for any one participant but counterbalanced across participants for the experiment. The order of task presentation was counterbalanced across participants.
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26. 15O administrations was 8 min. The data were acquired in one 90-s frame, beginning 5 s before the rising phase of the head curve. Correction for attenuation was made with a transmission scan collected at the beginning of each study. Images were reconstructed by filtered back projection (Hanning filter, cut off frequency of 0.5 cycles per pixel) into 63 image planes (separation 2.4 mm) and into a 128 by 128 pixel image matrix (size 2.1 mm). For data analysis we used the general linear model and theory of Gaussian fields, as implemented in SPM96 (Wellcome Department of Cognitive Neurology, London, UK). Images were realigned with the first as a reference, and then stereotactically transformed into the space of Talairach and Tournoux [J. Talairach and P. Tournoux, Co-Planar Stereotaxic Atlas of the Human Brain (Thieme, New York, 1988)]. The images were smoothed with a Gaussian filter of 12-mm full-width half maximum. Statistical parametric maps were derived with prespecified contrasts between images as discussed in the text [K. J. Friston et al., Hum. Brain Mapp. 2, 165 (1994); K. J. Friston et al., ibid. 3, 189 (1995)].
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28. The reaction time (RT) for correct responses for the color, orientation, and conjunction tasks was 352 ms (standard deviation 86 ms), 350 ms (standard deviation 95 ms), and 368 ms (standard deviation 104 ms), respectively. This significant difference in RT between conjunction and feature tasks is not in accord with Treisman's feature integration theory, if one regards our task as a conjunction search without distractors. However, similar elevated RTs in a conjunction search without distractors have been seen in the only functional imaging study previously reported of conjunction search (6). The RT declined with increasing rate of presentation, being 378 ms, 358 ms, 346 ms, and 357 ms for rates of 30, 50, 70, and 90 ellipses per minute, respectively. This may reflect participants finding it easier to stay "on task" at higher rates, keeping relevant behavioral goals more active. Error rates were highest (15.5%) with the color condition; for the orientation condition there were 5.05% errors, and for the conjunction condition 6.98% errors averaged over all participants. There is thus no suggestion from the error data that increased difficulty of the conjunction task might account for our results.
29. Tonic effects were indexed as an increase in baseline activity without an alteration of the correlation between activity and presentation rate. Phasic effects were indexed as a change in the correlation of activity and presentation rate. See Fig. 1 and Table 2.
30. The Z score was 4.22, Talairach coordinates (42 22 40), and P < 0.001 uncorrected for multiple comparisons because of our prior hypothesis.
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41. BA 8 in monkey contains the frontal eye fields, and an alternate explanation for our results is that eye movements were responsible for the differences in neural activity between conjunction and feature tasks. However all stimuli were presented in an identical fashion over all tasks at fixation, and there is no reason to suspect differential eye movements in the conjunction condition. Furthermore, in humans the reported coordinates for the frontal eye fields are not located within BA 8 [T. Paus, Neuropsychologia 34, 475 (1996); G. A. O'Driscoll et al., Proc. Natl. Acad. Sci. U.S.A. 92, 925 (1995); P. T. Fox et al., Neurophysiology 54, 349 (1985).
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46. E. K. Miller and R. Desimone, Science 263, 520 (1994); E. K. Miller, L. Li, R. Desimone, J. Neurosci. 13, 1460 (1993); Science 254, 1377 (1991). "Adaptive mnemonic filtering" refers to the reduction in the response from a cell to a stimulus, which has been observed independently of task. However an extrapolation from single-cell data to the evoked hemodynamic response from activity in a population of neurons should be made with caution. Other effects are also seen in inferior temporal cells; for example, an enhancement of response to a stimulus when it matches a searched for target. Our data suggest that the aggregate outcome of activity in several subsets of neurons with different response characteristics is an overall decrease in inferior temporal activity.
47. E. K. Miller and R. Desimone, Science 263, 520 (1994); E. K. Miller, L. Li, R. Desimone, J. Neurosci. 13, 1460 (1993); Science 254, 1377 (1991). "Adaptive mnemonic filtering" refers to the reduction in the response from a cell to a stimulus, which has been observed independently of task. However an extrapolation from single-cell data to the evoked hemodynamic response from activity in a population of neurons should be made with caution. Other effects are also seen in inferior temporal cells; for example, an enhancement of response to a stimulus when it matches a searched for target. Our data suggest that the aggregate outcome of activity in several subsets of neurons with different response characteristics is an overall decrease in inferior temporal activity.
48. There are intriguing parallels with single-cell electrophysiology work, where both tonic and phasic signals are seen in inferior temporal cortex cells when monkeys attend to stimuli [(25); B. J. Richmond and T. Sato, Soc. Neurosci. Abstr. 8, 812 (1982); J. Neurophysiol. 58, 1292 (1987)]. However, there are important differences with our data; in terms of modulation by attention our data suggest only a tonic modulation of inferior temporal cortical activity. There is no phasic modulation by attention (Fig. 1). Rather, we see a correlation between the rate of presentation of stimuli and inferior temporal cortex activity in addition to the attention-related modulation of this activity.
49. There are intriguing parallels with single-cell electrophysiology work, where both tonic and phasic signals are seen in inferior temporal cortex cells when monkeys attend to stimuli [(25); B. J. Richmond and T. Sato, Soc. Neurosci. Abstr. 8, 812 (1982); J. Neurophysiol. 58, 1292 (1987)]. However, there are important differences with our data; in terms of modulation by attention our data suggest only a tonic modulation of inferior temporal cortical activity. There is no phasic modulation by attention (Fig. 1). Rather, we see a correlation between the rate of presentation of stimuli and inferior temporal cortex activity in addition to the attention-related modulation of this activity.
50. An alternate explanation for the modulatory effect seen in inferior temporal cortex might be that it reflects differences in the stimuli presented. Activity decreases in inferotemporal cortex units in monkey have been observed associated with target identification, and also with repetition of visual items [for example, (29)]. The probability of a target was kept constant at 50% in our study, and targets were physically identical in the conjunction condition but shared one feature in the feature tasks; therefore, there were more repetitions of physically identical targets per unit time in the conjunction task. However, if unequal repetition probabilities were to have an effect on our results, they should have led to increased activity with increasing rate of presentation. Such an effect would lead to a change in the slope relating rCBF to presentation rate in conjunction and feature tasks. We found no such evidence; the modulatory effect is tonic and so is task-dependent and stimulus-independent.
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58. We are grateful to the Wellcome Trust for their support, and to all our colleagues in the Functional Imaging Laboratory for their help in the conduct of this study. We also would like to thank D. Passingham, M. Husain, and our anonymous reviewers for their helpful comments and discussion.