Stimulus probability directs spatial attention: an enhancement of sensitivity in humans and monkeys

We examined whether improvements in sensory processing, defined as changes in sensitivity, could be elicited in a simple luminance discrimination task without eliciting concomitant changes in decision processing. To this end we developed a task, for use in both humans and monkeys, in which prior knowledge about where a discriminative stimulus was likely to appear (1) offered no decisional advantage in solving our task and (2) could be parametrically varied to yield a psychometric function. We found that if we parametrically varied the quality of prior knowledge, by increasing the probability, and thus the certainty, that a discriminative stimulus would appear at a particular location under these conditions, luminance discrimination improved for both human and monkey subjects. This improvement was correlated with an enhancement in sensory processing, but not with any systematic changes in decisional processing, as assessed by signal detection theory. These results suggest that (1) sensory processing and decision processing can be separated by task design and (2) systematic changes in prior knowledge about where a stimulus may appear can lead to systematic changes in sensitivity; providing a psychometric function for the influence of prior knowledge on perceptual sensitivity. Importantly, these results were obtained from both human and monkey subjects. Similar task designs could be used in physiological studies attempting to generate linking hypotheses between psychometric and neurometric functions, ultimately allowing changes in perceptual sensitivity to be linked to changes in an underlying neural substrate.

[1]  H. Hawkins,et al.  Visual attention modulates signal detectability. , 1990, Journal of experimental psychology. Human perception and performance.

[2]  R J Herrnstein,et al.  Formal properties of the matching law. , 1974, Journal of the experimental analysis of behavior.

[3]  Raja Parasuraman,et al.  Varieties of attention , 1984 .

[4]  R. Andersen,et al.  Change in motor plan, without a change in the spatial locus of attention, modulates activity in posterior parietal cortex. , 1998, Journal of neurophysiology.

[5]  H. Schiffman Sensation and Perception: An Integrated Approach , 1976 .

[6]  ● Pytorch,et al.  Attention! , 1998, Trends in Cognitive Sciences.

[7]  P. Glimcher,et al.  Responses of intraparietal neurons to saccadic targets and visual distractors. , 1997, Journal of neurophysiology.

[8]  G Sperling,et al.  The attention operating characteristic: examples from visual search. , 1978, Science.

[9]  John H. R. Maunsell,et al.  Attentional modulation of visual motion processing in cortical areas MT and MST , 1996, Nature.

[10]  M N Shadlen,et al.  Motion perception: seeing and deciding. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[11]  R. Andersen,et al.  Motor intention activity in the macaque's lateral intraparietal area. I. Dissociation of motor plan from sensory memory. , 1996, Journal of neurophysiology.

[12]  C. J. Downing Expectancy and visual-spatial attention: effects on perceptual quality. , 1988, Journal of experimental psychology. Human perception and performance.

[13]  J. Findlay,et al.  Sensitivity and criterion effects in the spatial cuing of visual attention , 1987, Perception & psychophysics.

[14]  J. Palmer,et al.  Measuring the effect of attention on simple visual search. , 1993, Journal of experimental psychology. Human perception and performance.

[15]  R. Duncan Luce,et al.  Individual Choice Behavior , 1959 .

[16]  A. Fuchs,et al.  A method for measuring horizontal and vertical eye movement chronically in the monkey. , 1966, Journal of applied physiology.

[17]  M. Posner,et al.  Attention and the detection of signals. , 1980, Journal of experimental psychology.

[18]  William C. Ogden,et al.  Attended and unattended processing modes: The role of set for spatial location , 2014 .

[19]  M. Goldberg,et al.  Representation of visuomotor space in the parietal lobe of the monkey. , 1990, Cold Spring Harbor symposia on quantitative biology.

[20]  K. Nakayama,et al.  Priming of pop-out: II. The role of position , 1996, Perception & psychophysics.

[21]  R. Andersen Encoding of intention and spatial location in the posterior parietal cortex. , 1995, Cerebral cortex.

[22]  Michael L. Platt,et al.  Neural correlates of decision variables in parietal cortex , 1999, Nature.

[23]  R. Marrocco,et al.  Visual orienting and alerting in rhesus monkeys: comparison with humans , 1996, Behavioural Brain Research.

[24]  M. Shaw,et al.  Optimal allocation of cognitive resources to spatial locations. , 1977, Journal of experimental psychology. Human perception and performance.

[25]  M. Goldberg,et al.  Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. , 1996, Journal of neurophysiology.

[26]  M. Carrasco,et al.  Spatial covert attention increases contrast sensitivity across the CSF: support for signal enhancement , 2000, Vision Research.

[27]  R. Andersen,et al.  Coding of intention in the posterior parietal cortex , 1997, Nature.

[28]  K. Nakayama,et al.  Priming of pop-out: I. Role of features , 1994, Memory & cognition.

[29]  M. Goldberg,et al.  The representation of visual salience in monkey parietal cortex , 1998, Nature.

[30]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  R. Andersen,et al.  Spatially tuned auditory responses in area LIP of macaques performing delayed memory saccades to acoustic targets. , 1996, Journal of neurophysiology.

[32]  K. H. Britten,et al.  Neuronal correlates of a perceptual decision , 1989, Nature.

[33]  R. A. Kinchla Temporal and channel uncertainty in detection: A multiple observation analysis , 1969 .

[34]  Richard C. Atkinson,et al.  Stimulus Sampling Theory , 1967 .

[35]  W. Newsome,et al.  Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  Vision Research , 1961, Nature.

[37]  L. Kaufman,et al.  Handbook of perception and human performance , 1986 .

[38]  S J Luck,et al.  Mechanisms of visual-spatial attention: resource allocation or uncertainty reduction? , 1996, Journal of experimental psychology. Human perception and performance.

[39]  Howard S. Bashinski,et al.  Enhancement of perceptual sensitivity as the result of selectively attending to spatial locations , 1980, Perception & psychophysics.

[40]  R. Andersen,et al.  Motor intention activity in the macaque's lateral intraparietal area. II. Changes of motor plan. , 1996, Journal of neurophysiology.

[41]  Neil A. Macmillan,et al.  Detection Theory: A User's Guide , 1991 .

[42]  C L Colby,et al.  The analysis of visual space by the lateral intraparietal area of the monkey: the role of extraretinal signals. , 1993, Progress in brain research.

[43]  G W Humphreys,et al.  Luminance-increment detection: capacity-limited or not? , 1991, Journal of experimental psychology. Human perception and performance.

[44]  B. C. Motter Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. , 1993, Journal of neurophysiology.

[45]  Stefan Treue,et al.  Feature-based attention influences motion processing gain in macaque visual cortex , 1999, Nature.

[46]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[47]  A. Parker,et al.  Sense and the single neuron: probing the physiology of perception. , 1998, Annual review of neuroscience.

[48]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[49]  S J Luck,et al.  Effects of spatial cuing on luminance detectability: psychophysical and electrophysiological evidence for early selection. , 1994, Journal of experimental psychology. Human perception and performance.

[50]  W. Estes The cognitive side of probability learning. , 1976 .

[51]  Daniel G Bobrow,et al.  On data-limited and resource-limited processes , 1975, Cognitive Psychology.

[52]  M. Shadlen,et al.  Exploring the Neurophysiology of Decisions , 1998, Neuron.

[53]  H. Schiffman Sensation and perception: An integrated approach, 3rd ed. , 1990 .

[54]  Marilyn L Shaw,et al.  Attending to multiple sources of information: I. The integration of information in decision making , 1982, Cognitive Psychology.

[55]  R A Kinchla,et al.  Precue effects in visual search: Data or resource limited? , 1995, Perception & psychophysics.

[56]  B. Dosher,et al.  External noise distinguishes attention mechanisms , 1998, Vision Research.