SOKENDAI physiology lecture course 2013 "Neuroscience of Cognition and Motor control" #4

"Attention and Motor Control"

May 24, Friday 10:00-12:00, Myodaiji Staff Hall 2F Meeting room Masatoshi Yoshida (NIPS and SOKENDAI, Assistant professor)

1. Introduction 1-1. What is attention? -- Let’s start from examples • We cannot consciously perceive a big change

in a scene when we do not pay attention to it. • Attention has a strong influence on what we

see. 1-2. Definition of attention • William James (Principles of Psychology

(1890)): "Everyone knows what attention is. It is the taking possession by the mind in clear and vivid form, of one out of what seem several simultaneously possible objects...It implies withdrawal from some things in order to deal effectively with others..."

1.3 Taxonomy of attention • Two kinds of attention • Selective attention: ability to focus on

positions or objects • Sustained attention: alertness, ability to

concentrate • What drives selective attention? • Bottom-up: stimulus-driven (pre-attentive,

pop-out) • Top-down: goal-directed

• What is selected in selective attention? • Position: spatial attention • Object (feature): object (feature)-based

attention • Bottom-up vs. top-down attention in pre-cue

task • Bottom-up attention1 • Top-down attention

2. Attention and eye movements

2-1. Neural network for attention and saccadic eye movements • Brain regions involved in bottom-up attention • Brain regions involved in top-down attention2 • Brain regions involved in saccadic eye

movements 2-2. Overt attention and covert attention in human • Overt attention and Covert attention3 • Overt selection of visual features contained

within a portrait as revealed by the scanning eye movements.

• The female monkey on the left is looking straight ahead. However, it is apparent that she is fully attending to her neighbor.

• Overt attention and covert attention activate the same brain regions. 4,5

2-3. Overt attention and covert attention in monkey • Saccade control system • FEF: frontal eye field (premotor cortex for

eye) • SC: superior colliculus (one of the midbrain

structures) • FEF is involved in covert attention6 • Electrical stimulation to FEF directs covert

attention without evoking saccades. • SC is involved in covert attention7 • Inactivation of SC leads to deficits in covert

attention but does not affect MT and MST. • The effect of inactivation is not an indirect

effect on MT/MST but a direct effect on SC (or FEF).

• Cortex is not necessary for attention!

3. Dorsal and ventral attention network 3-1. Dorsal and ventral attention network in human • When top-down attention is manipulated by

pre-cue, both dorsal and ventral attention systems are activated.8

• Note these are NOT the dorsal and ventral visual pathway

• Resting state BOLD activity8 • Strong and significant positive temporal

correlation of spontaneous activity at rest. • The dorsal network is anti-correlated with the

default network. 3-2. Spatial hemineglect as a disorder of attentional network • What is 'spatial hemineglect'? • The inability to report, respond, or orient to

stimuli in the contralesional space. • The deficit must not be fully attributable to

primary sensory deficits (e.g., hemianopia) or motor disturbance (e.g., hemiparesis).

• Neglect occurs more commonly in those with brain injury affecting the right cortical hemisphere.

• Where is the key lesion site? • Hemineglect as a disorder of network9 • Activity of MFG and STS shows a sign of

recovery in the chronic period. • However, functional connectivity did not

recover in the chronic period. 3-3. Ventral attention network in monkey? • The ventral attention system (TPJ-IFG) is not

identified in monkeys. • Monkeys have no BA40 (TPJ/SMG). • (Putative BA40 is part of BA7).

• The dorsal network may be mediated by SLFII. • SLF(the superior longitudinal fasciculus)

• SLFII: spatial attention and spatial awareness

• The ventral network may be mediated by AF (the arcuate fasciculus).10

• AF connection is very sparse in macaque11

4. Saliency computational model 4-1. What is saliency map? • What is saliency? • salient (adj): “very easy to notice” • visual salience (or visual saliency): the

distinct subjective perceptual quality which makes some items in the world stand out from their neighbors and immediately grab our attention.(Scholarpedia by Laurent Itti)

• What grabs our attention? • Where is the object that is different from the

rest? • Feature integration theory12 • Original computational model13 • A unique saliency map, independent of

features • Winner-take-all rule (WTA) • Selection was made on the saliency map

• What is saliency map? • An explicit 2D map that encodes the saliency

of objects in the visual environment • A computational concept

• Saliency computational model14 • Iterative calculation of center-surround

differentiation and normalization • Intracortical lateral inhibition is

mathematically equivalent to second derivative (=laplacian). It is used for edge detection.

4-2. Applications of the saliency model • Application #1: Modeling visual search • Application #2: Advertisement • AD people collect eye-tracking data to

evaluate the effect of advertisement. • But it is expensive and time-consuming. • You do not need to collect eye-tracing data if

you use the saliency model instead. • Now it is commercially available.

4-3. Saliency map in the brain • Brain network involved in saliency 4-4: Saliency map in the brain - Parietal cortex • Temporal saliency drives LIP neurons15 • Visual information (stimuli in RF) is

sufficient? • Or saliency (abrupt onset of stimuli) is

necessary? • Stimuli with low saliency (stable stimuli) did

not drive a LIP neuron. • Visual information (stimuli in RF) is not

enough! • Stimuli with high salience (recently flashed

stimuli) drive a LIP neuron. • LIP represents visual salience.

• Decoding saliency from the brain16 • The difference of saliency in four quadrants

can be decoded from pIPS and early visual cortex.

4-5: Saliency map in the brain - Is V1 necessary? • Computational model predicts monkey’s gaze • Salient stimuli attract gazes of blindsight

monkeys17 • The gaze positions have higher saliency,

than expected from random eye movement. • Revised view of saliency computation 4-6: Clinical application 1 - ADHD • Classification of neurological disorders18 • Eye-tracking (20min) is sufficient to classify

subjects, if combined with the saliency model.

4-7: Clinical application 2 - autism • Autistic people do not look at eyes. But why? • Visual saliency of eyes and mouth matters.19

• The authors generated many images with different saliency for eyes and mouth.

• The autistic people see the mouth even when the saliency is low.

• The autistic people do not avoid the eyes. Rather, they preferentially look at the mouth.

4-8: Clinical application 3 - schizophrenia • Aberrant salience hypothesis of psychosis20

5. Summary • Attention and eye movements share the same

brain circuitry. • Dorsal and ventral attentional networks are

identified in humans (but not yet in monkeys). • Saliency computational model is able to

predict gaze of humans and monkeys.

References 1. Ikeda, T., Yoshida, M. & Isa, T. Lesion of primary

visual cortex in monkey impairs the inhibitory but not the facilitatory cueing effect on saccade. Journal of Cognitive Neuroscience 23, 1160–1169 (2011).

2. Baluch, F. & Itti, L. Mechanisms of top-down attention. Trends in Neurosciences 34, 210–224 (2011).

3. Moore, T., Armstrong, K. M. & Fallah, M. Visuomotor origins of covert spatial attention. Neuron 40, 671–683 (2003).

4. Beauchamp, M. S., Petit, L., Ellmore, T. M., Ingeholm, J. & Haxby, J. V. A parametric fMRI study of overt and covert shifts of visuospatial attention. NeuroImage 14, 310–321 (2001).

5. de Haan, B., Morgan, P. S. & Rorden, C. Covert orienting of attention and overt eye movements activate identical brain regions. Brain Research 1204, 102–111 (2008).

6. Moore, T. & Fallah, M. Control of eye movements and spatial attention. Proc Natl Acad Sci USA 98, 1273–1276 (2001).

7. Zénon, A. & Krauzlis, R. J. Attention deficits without cortical neuronal deficits. Nature 489, 434–437 (2012).

8. Corbetta, M. & Shulman, G. L. Spatial neglect and attention networks. Annu. Rev. Neurosci. 34, 569–599 (2011).

9. He, B. J. et al. Breakdown of Functional Connectivity in Frontoparietal Networks Underlies Behavioral Deficits in Spatial Neglect. Neuron 53, 905–918 (2007).

10. Petrides, M. & Pandya, D. N. Distinct Parietal and Temporal Pathways to the Homologues of Broca's Area in the Monkey. Plos Biol 7, e1000170 (2009).

11. Rilling, J. K. et al. The evolution of the arcuate fasciculus revealed with comparative DTI. Nat Neurosci 11, 426–428 (2008).

12. Treisman, A. Feature binding, attention and object perception. Philosophical Transactions of the Royal Society B: Biological Sciences 353, 1295–1306 (1998).

13. Koch, C. & Ullman, S. Shifts in selective visual attention: towards the underlying neural circuitry. Hum Neurobiol 4, 219–227 (1984).

14. Itti, L. & Koch, C. Computational modelling of visual attention. Nat Rev Neurosci 2, 194–203 (2001).

15. Gottlieb, J. P., KUSUNOKI, M. & Goldberg, M. E. The representation of visual salience in monkey parietal cortex. Nature 391, 481–484 (1998).

16. Bogler, C., Bode, S. & Haynes, J.-D. Decoding successive computational stages of saliency processing. Curr. Biol. 21, 1667–1671 (2011).

17. Yoshida, M. et al. Residual attention guidance in blindsight monkeys watching complex natural scenes. Current Biology 22, 1429–1434 (2012).

18. Tseng, P.-H. et al. High-throughput classification of clinical populations from natural viewing eye movements. J Neurol 1–10 (2012). doi:10.1007/s00415-012-6631-2

19. Neumann, D., Spezio, M. L., Piven, J. & Adolphs, R. Looking you in the mouth: abnormal gaze in autism resulting from impaired top-down modulation of visual attention. Social Cognitive and Affective Neuroscience 1, 194–202 (2006).

20. Kapur, S. How antipsychotics become anti-‘psychotic’--from dopamine to salience to psychosis. Trends Pharmacol. Sci. 25, 402–406 (2004).