* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
Download Neural coding of behavioral relevance in parietal cortex
Mirror neuron wikipedia , lookup
Stroop effect wikipedia , lookup
Activity-dependent plasticity wikipedia , lookup
Response priming wikipedia , lookup
Environmental enrichment wikipedia , lookup
Effects of sleep deprivation on cognitive performance wikipedia , lookup
Human brain wikipedia , lookup
Development of the nervous system wikipedia , lookup
Functional magnetic resonance imaging wikipedia , lookup
Affective neuroscience wikipedia , lookup
Neuroplasticity wikipedia , lookup
Emotional lateralization wikipedia , lookup
Nervous system network models wikipedia , lookup
Optogenetics wikipedia , lookup
Psychophysics wikipedia , lookup
Cortical cooling wikipedia , lookup
Cognitive neuroscience of music wikipedia , lookup
Neuropsychopharmacology wikipedia , lookup
Eyeblink conditioning wikipedia , lookup
Neural coding wikipedia , lookup
Stimulus (physiology) wikipedia , lookup
Neuroeconomics wikipedia , lookup
Synaptic gating wikipedia , lookup
Visual search wikipedia , lookup
Premovement neuronal activity wikipedia , lookup
Executive functions wikipedia , lookup
Visual extinction wikipedia , lookup
Metastability in the brain wikipedia , lookup
Aging brain wikipedia , lookup
Neuroanatomy of memory wikipedia , lookup
Time perception wikipedia , lookup
Neuroesthetics wikipedia , lookup
Inferior temporal gyrus wikipedia , lookup
C1 and P1 (neuroscience) wikipedia , lookup
Neural correlates of consciousness wikipedia , lookup
Feature detection (nervous system) wikipedia , lookup
194 Neural coding of behavioral relevance in parietal cortex John A Assad Flexible control of behavior requires the selective processing of task-relevant sensory information and the appropriate linkage of sensory input to action. A great deal of evidence suggests a central role for the parietal cortex in these functions. Recent results from neurophysiological studies in non-human primates and neuroimaging experiments in humans illuminate the importance of parietal cortex for attention, and suggest how parietal neurons might allow the dynamic representation of behaviorally relevant information. Addresses Department of Neurobiology, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA e-mail: [email protected] Current Opinion in Neurobiology 2003, 13:194–197 This review comes from a themed issue on Cognitive neuroscience Edited by Brian Wandell and Anthony Movshon 0959-4388/03/$ – see front matter ß 2003 Elsevier Science Ltd. All rights reserved. DOI 10.1016/S0959-4388(03)00045-X Abbreviations fMRI functional magnetic resonance imaging IPS intraparietal sulcus LIP lateral intraparietal area MST medial superior temporal area MT middle temporal area RF receptive field VIP ventral intraparietal area Introduction It could be argued that a general function of the cerebral cortex is to facilitate the association of sensory input with particular behaviors. This implies that relevant information is first selectively extracted from the sensory scene, and then linked to actions in a manner appropriate to the demands of the task at hand. For example, under different circumstances we can selectively attend to specific attributes of a visual scene — say red objects — yet respond to them differently, such as by reaching to acquire a ripe apple in a tree or by extending a foot to apply the brakes in response to a stoplight. Decades of neuropsychological research point to a role of the parietal cortex in these processes, particularly in visually guided behaviors. Patients with parietal lesions are not blind per se, but they have deficits in their representation of and their attention to the spatial attributes of their visual surroundings, and in their use of Current Opinion in Neurobiology 2003, 13:194–197 visual information to guide movements of the body [1–3]. Physiological studies in non-human primates and neuroimaging studies in human subjects [4] have confirmed that individual parietal neurons and cortical areas are activated during spatial, attentional, and visuomotor behaviors. Mountcastle and co-workers [5] were the first to identify neurons throughout the monkey parietal lobe that were activated by a host of visually guided behaviors of the eyes or hands. Later studies identified parietal activity that was related to attention to or salience of particular locations [6–8], and the intention to make eye or hand movements to those locations [9,10]. In addition, many neurons in parietal areas in the monkey are sensitive to spatial attributes of visual stimuli, such as the direction of motion [11–13], and are likely to contribute to the initiation or maintenance of behaviors made to acquire moving targets, such as pursuit eye movements [14,15]. The purpose of this review is to discuss recent findings that expand our understanding of the role of parietal cortex in encoding behavioral relevance. New experiments have addressed how attention modulates parietal responses, how physiological modulation by attention relates to behavioral enhancement, and how non-spatial information can be dynamically represented depending on the demands of the task. Parietal mechanisms of attention revealed by single-unit studies Some of the most detailed experiments on the neuronal mechanisms of attention in the parietal pathway have been carried out in the middle temporal area (MT) and the medial superior temporal area (MST) of the monkey. MT and MST contain a preponderance of neurons that are selective for the direction of moving stimuli within their receptive fields (RF). Treue and Maunsell [16,17] were the first to show that the direction-selective responses of many MT and MST neurons were modulated by attention. Neuronal responses to stimuli moving within the RF are generally larger when the animal attends to the location of the RF. Attentional effects are not solely restricted to attended locations, however [18,19]. For example, if an animal attends to a stimulus moving in a particular direction, neuronal responses to a second stimulus can be enhanced if that stimulus moves in the same direction as the attended stimulus [18]. Attention also generally ‘scales’ neuronal responses by a uniform factor regardless of whether the visual stimulus moves in a preferred or non-preferred direction for a given neuron [18]. These results suggest that attention exerts a multiplicative modulation of neuronal responses — an effect that is also common to neurons in the temporal www.current-opinion.com Parietal cortex and behavioral relevance Assad 195 visual pathways [20,21]. To test this idea further, Martinez-Trujillo and Treue [22] examined attentional effects in MT as a function of the luminance contrast of a moving stimulus relative to a dark background. Increasing stimulus contrast also tends to increase neuronal responses in a scalar, multiplicative fashion [23]. Attention caused a shift in the sigmoidal contrast–response function of the neurons, implying that the neurons were most sensitive to both attention and changing contrast at intermediate contrast levels [22]. Thus, the mechanisms of attention may be similar or identical to the mechanisms that determine the strength of visual stimuli. Comparing neuronal and behavioral effects of attention Spatial attention confers a variety of behavioral advantages, such as decreased reaction time in visual detection tasks [24–26]. A challenging issue has been to understand how attentional modulation of neural activity could give rise to the behavioral effects of attention. Cook and Maunsell [27] have directly examined this question by determining the attentional modulation of neuronal responses in the MT and the ventral intraparietal area (VIP), while simultaneously measuring the effects of spatial attention on performance in a motion-detection task. Monkeys had to detect a change in motion coherence in one of two spatially distinct patches of moving dots, when they were directed in advance to attend to the appropriate or inappropriate patch. Withdrawing attention from the stimulus decreased the animals’ ability to detect the change in motion coherence, and also reduced neuronal responses in MT and VIP. Interestingly, the changes in neuronal responses in MT were generally too small to account for the behavioral changes, whereas the changes in VIP responses were generally stronger than expected to explain the behavioral effect. These results suggest that comparing the neuronal and behavioral effects of attention may be a reasonable way to gauge the importance of parietal areas for particular visual behaviors. Other studies have examined the link between neuronal and behavioral modulation less directly. For example, it has been known for a long time that a difficult task could increase the responses of neurons, presumably by demanding more attention to relevant stimuli [28]. Other experiments suggest that attention can increase or decrease responses to task-relevant stimuli depending on the way that attention is allocated. For example, Constantinidis and Steinmetz [29,30] recorded from parietal area 7a during a task in which monkeys had to localize an odd-colored stimulus spot amidst an array of spots extending inside and outside of the RF. The presence of a non-salient spot in the RF elicited little response. If the salient spot was within the RF, the response of neurons was much stronger and comparable to that when a single spot was presented alone at the same location [29]. In contrast, if the animals were cued in www.current-opinion.com advance to attend to the same location in the RF, later presentations at that location produced smaller responses [30]. This suggests that parietal areas similar to 7a may be involved in the re-direction of attention, for example by responding to salient stimuli, but less involved in the maintenance of attention to particular locations. Similar results have also been reported for the lateral intraparietal area (LIP) [31,32]. Neuroimaging studies and parietal mechanisms of attention Recent neuroimaging studies conducted on human subjects continue to provide evidence of the parietal lobe’s role in encoding behavioral relevance [4,33]. Culham et al. [34] used functional magnetic resonance imaging (fMRI) to assess the role of different brain regions in attentional tracking. Subjects were instructed to maintain gaze at a fixed location while covertly tracking the position of one or more spots moving randomly within a patch of visual space. The number of tracked stimuli was increased to examine whether the activity of a particular brain region was affected by the attentional ‘load’ or rather reflected the immediate demands of the task, such as planning eye movements to one of the moving targets. Within the parietal lobe, areas in the intraparietal sulcus (IPS) and the inferior parietal lobule showed load-related changes in metabolic activity, suggesting their involvement in the specific attentional demands of the task. MT/MST showed little effect of attentional load, consistent with previous findings [35] that MT/MST is not specifically activated by attentional tracking. Interestingly, these results agree with those of a recent neuropsychological study [36]. This study suggests that patients with parietal lesions that spare the MT/MST complex are severely impaired in attentional tracking and other high-level motion tasks, but are not deficient in low-level motion tasks [36]. fMRI has also been used to address the exact role of the parietal areas in attention, in particular whether parietal cortex is involved in maintaining attention to specific spatial locations or rather in providing a transient signal when attention is shifted from one location to another. Yantis et al. [37] directed subjects to detect a stimulus in one of two rapid serial visual displays presented simultaneously in opposite visual hemifields. Attention was rapidly shifted between the opposite hemifields in response to particular stimuli appearing on the attended side. Many extrastriate visual areas showed sustained increases in activity for attention to the contralateral visual field, whereas areas in the right superior and inferior parietal lobules showed transient activation whenever attention was reallocated. Other areas in the left IPS showed the sustained pattern of activity for attention to the contralateral field. These results suggest that dynamic and static aspects of spatial attention could be subserved by distinct parietal areas. Current Opinion in Neurobiology 2003, 13:194–197 196 Cognitive Neuroscience Several other recent fMRI experiments suggest a specialization of the parietal cortex in dynamic attention. Shulman et al. [38] compared neural activity in the parietal cortex when subjects performed either a color or a motion match-to-sample task that were visually identical. The left parietal cortex was selectively activated when subjects performed the motion task and when the subjects alternated rapidly between the two tasks, which suggests that left parietal areas might also contribute to specifying the switching of task demands. Task-switching signals may be localized to the lateral portion of the IPS [39]. Attentional processes in the IPS appear to extend to other stimulus modalities beyond vision. For example, a positron-emission tomography (PET) study found signals in the IPS when subjects attended to either contralateral visual stimuli or somatosensory stimuli [40]. Dynamic representation of non-spatial features in the parietal cortex As described above, attentional effects are not just restricted to the location of visual stimuli. Saenz et al. [41] asked subjects to attend to a patch of moving dots in one hemifield, while simultaneously viewing a second task-irrelevant patch of moving dots in the opposite hemifield. fMRI signals in response to the irrelevant stimulus were larger when their movement was in the same direction as the attended stimulus. Among extrastriate visual areas, feature-based attention was particularly strong in MT [41], a similar result to that of experiments described above in monkey MT [18]. If attention to a non-spatial attribute (such as direction) can ‘spread’ to an ignored stimulus, what would happen if instead the non-spatial feature were behaviorally relevant? In particular, would the parietal cortex represent a non-spatial feature if it were relevant for a behavior that is known to engage parietal areas, such as an eye movement? Toth and Assad [42] examined this issue by training monkeys to use a colored visual cue to direct a saccadic eye movement. Neuronal responses were recorded in the LIP. On alternate blocks of trials, the animals used either the cue’s color or location (irrespective of color) to direct a saccade towards or away from the response field of the LIP neuron under study. Surprisingly, many LIP neurons responded to the cue in a manner that was selective for the cue’s color. This was unexpected, as dorsal visual stream neurons, including parietal neurons, have not been reported to be selective for color. However, the color selectivity of the LIP neurons was only present when color was relevant to solving the task: that is, the same neurons were not color selective when the cue location was the task-relevant feature — even though the task was otherwise visually identical. Taken together, these data suggest that stimulus representations in the parietal cortex can adapt to reflect the task’s demands. Current Opinion in Neurobiology 2003, 13:194–197 Conclusions Recent experiments provide a subtle and detailed view of how neuronal activity in the parietal cortex reflects behavioral relevancy. However, many important questions remain. A crucial issue is to gain an understanding of the cellular mechanisms underlying attention. For example, what can we infer about the mechanism(s) of attention given its multiplicative, modulatory nature? Similarly, what is the mechanistic relevance of the similarities between attentional modulation and changing the stimulus strength? These questions are closely entwined with the problem of how attention is allocated. In particular, the new data might suggest that attention reflects a local selective transfer of information between brain areas, rather than the oft-suggested (and rather awkward) idea that attention is centrally ‘gated’. A related issue, especially for animals trained by operant conditioning, is to understand the similarities and distinctions between attention and reward mechanisms [43,44]. Finally, neuroimaging has provided an important complement to neurophysiological studies in animals, enabling us to understand more global patterns of brain activity associated with attention. Future investigations on attention should aim to provide a more integrated view of these two experimental approaches. References and recommended reading Papers of particular interest, published within the annual period of review, have been highlighted as: of special interest of outstanding interest 1. Critchley M: The Parietal Lobes. New York: Hafner; 1953. 2. Andersen RA: Inferior parietal lobule in spatial perception and visuomotor integration. In The Handbook of Physiology, Sec. 1: The Nervous System Vol. 5, Higher Functions of the Brain Part 2. Edited by Plum F, Mountcastle VB, Geiger SR. Bethesda: Am Physiol Soc; 1987:483-518. 3. Feinberg TE, Farah MJ: Behavioral Neurology and Neuropsychology. New York: McGraw-Hill; 1997. 4. Culham JC, Kanwisher NG: Neuroimaging of cognitive functions in human parietal cortex. Curr Opin Neurobiol 2001, 11:157-163. 5. Mountcastle VB, Lynch JC, Georgopoulos AP, Sakata S, Acuna CL: Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. J Neurophysiol 1975, 38:871-908. 6. Bushnell MC, Goldberg ME, Robinson DL: Behavioral enhancement of visual responses in monkey cerebral cortex. I. Modulation in posterior parietal cortex related to selective visual attention. J Neurophysiol 1981, 46:755-771. 7. Colby CL, Duhamel JR, Goldberg ME: Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. J Neurophysiol 1996, 76:2841-2852. 8. Kusunoki M, Gottlieb J, Goldberg ME: The lateral intraparietal area as a salience map: the representation of abrupt onset, stimulus motion, and task relevance. Vision Res 2000, 40:1459-1468. 9. Snyder LH, Batista AP, Andersen RA: Coding of intention in the posterior parietal cortex. Nature 1997, 386:167-170. 10. Andersen RA: Encoding of intention and spatial location in the posterior parietal cortex. Cereb Cortex 1995, 5:457-469. 11. Andersen RA: Neural mechanisms of visual motion perception in primates. Neuron 1997, 18:865-872. www.current-opinion.com Parietal cortex and behavioral relevance Assad 197 12. Albright TD: Cortical processing of visual motion. Rev Oculomot Res 1993, 51:77-201. 13. Maunsell JHR, Newsome WT: Visual processing in monkey extrastriate cortex. Annu Rev Neurosci 1987, 10:363-401. 14. Newsome WT, Wurtz RH, Komatsu H: Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. J Neurophysiol 1988, 60:604-619. 15. Newsome WT, Pare EB: A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J Neurosci 1988, 8:2201-2211. 16. Treue S, Maunsell JH: Attentional modulation of visual motion processing in cortical areas MT and MST. Nature 1996, 382:539-541. 17. Treue S, Maunsell JH: Effects of attention on the processing of motion in macaque middle temporal and medial superior temporal visual cortical areas. J Neurosci 1999, 19:7591-7602. 18. Treue S, Martinez Trujillo JC: Feature-based attention influences motion processing gain in macaque visual cortex. Nature 1999, 399:575-579. 19. McAdams CJ, Maunsell JH: Attention to both space and feature modulates neuronal responses in macaque area V4. J Neurophysiol 2000, 83:1751-1755. 20. McAdams CJ, Maunsell JH: Effects of attention on orientationtuning functions of single neurons in macaque cortical area V4. J Neurosci 1999, 19:431-441. 21. Reynolds JH, Pasternak T, Desimone R: Attention increases sensitivity of V4 neurons. Neuron 2000, 26:703-714. 22. Martinez-Trujillo J, Treue S: Attentional modulation strength in cortical area MT depends on stimulus contrast. Neuron 2002, 35:365-370. The authors measured the strength of attentional modulation of MT neurons in the monkey as a function of stimulus contrast. Attentional modulation was strongest for intermediate contrasts within the cells’ dynamic range, and was considerably reduced at higher or lower contrasts. This shared non-linearity between the effect of attention and the effect of changing contrast suggests that the two processes could engage similar mechanisms. 31. Gottlieb JP, Kusunoki M, Goldberg ME: The representation of visual salience in monkey parietal cortex. Nature 1998, 391:481-484. 32. Powell KD, Goldberg ME: Response of neurons in the lateral intraparietal area to a distractor flashed during the delay period of a memory-guided saccade. J Neurophysiol 2000, 84:301-310. 33. Corbetta M, Shulman GL: Control of goal-directed and stimulusdriven attention in the brain. Nat Rev Neurosci 2002, 3:201-215. 34. Culham JC, Cavanagh P, Kanwisher NG: Attention response functions: characterizing brain areas using fMRI activation during parametric variations of attentional load. Neuron 2001, 32:737-745. The authors measured fMRI signals in fixating human subjects covertly tracking one or more moving dots amidst moving distracter dots. The subjects’ attentional ‘load’ was requiring them to track more dots. Activation of many parietal and frontal areas increased with the number of tracked dots, suggesting that they have a role in attentional processes. 35. Culham JC, Brandt SA, Cavanagh P, Kanwisher NG, Dale AM, Tootell RB: Cortical fMRI activation produced by attentive tracking of moving targets. J Neurophysiol 1998, 80:2657-2670. 36. Battelli L, Cavanagh P, Intriligator J, Tramo MJ, Henaff MA, Michel F, Barton JJ: Unilateral right parietal damage leads to bilateral deficit for high-level motion. Neuron 2001, 32:985-995. The authors examined motion perception in patients with right parietal lesions. The patients were unaffected in low-level motion tasks, but had severe deficits in detecting simple apparent motion in either visual field. These data support the theory that perceiving apparent motion requires attention. Moreover, given the importance of fine temporal resolution for perceiving apparent motion, the right parietal cortex might be specialized for attention to the precise timing of transient visual events. 23. Tolhurst DJ: Separate channels for the analysis of the shape and the movement of moving visual stimulus. J Physiol 1973, 231:385-402. 37. Yantis S, Schwarzbach J, Serences JT, Carlson RL, Steinmetz MA, Pekar JJ, Courtney SM: Transient neural activity in human parietal cortex during spatial attention shifts. Nat Neurosci 2002, 5:995-1002. Subjects attended to one of two rapid serial visual presentations placed on either side of the fixation point. Particular stimuli triggered the subjects either to continue maintaining attention to one side or to shift attention to the opposite hemifield. fMRI signals in many extrastriate visual areas were maintained throughout a period of maintained contralateral attention, but posterior parietal areas were transiently activated whenever attention shifted to either side. These data suggest that parietal cortex may be involved in shifting attention. 24. Posner MI: Orienting of attention. Quart J Exp Psych 1980, 32:3-25. 38. Shulman GL, d’Avossa G, Tansy AP, Corbetta M: Two attentional processes in the parietal lobe. Cereb Cortex 2002, 12:1124-1131. 25. Posner MI, Petersen SE: The attention system of the human brain. Annu Rev Neurosci 1990, 13:25-42. 39. Rushworth MF, Paus T, Sipila PK: Attention systems and the organization of the human parietal cortex. J Neurosci 2001, 21:5262-5271. 26. Desimone R, Duncan J: Neural mechanisms of selective visual attention. Annu Rev Neurosci 1995, 18:193-222. 27. Cook EP, Maunsell JH: Attentional modulation of behavioral performance and neuronal responses in middle temporal and ventral intraparietal areas of macaque monkey. J Neurosci 2002, 22:1994-2004. The authors trained monkeys to detect a change in the motion coherence of one of two patches of moving random dots. One of the patches was more likely to change throughout a block of trials. If the change occurred in the (implicitly) less-attended patch, there was a reduction in both behavioral performance and the responses of MT and VIP neurons with RF’s at that location. Quantitative comparisons of the neuronal and behavioral effects suggested that neither area was likely to be the key determinant for the behavioral effects of attention in that particular task. 28. Spitzer H, Desimone R, Moran J: Increased attention enhances both behavioral and neuronal performance. Science 1988, 240:338-340. 29. Constantinidis C, Steinmetz MA: Neuronal response in area 7a to multiple-stimulus display: I. neurons encode the location of the salient stimulus. Cereb Cortex 2001, 11:581-591. 30. Constantinidis C, Steinmetz MA: Neuronal responses in area 7a to multiple stimulus displays: II. responses are suppressed at the cued location. Cereb Cortex 2001, 11:592-597. www.current-opinion.com 40. Macaluso E, Frith CD, Driver JL: Directing attention to locations and to sensory modalities: multiple levels of selective processing revealed with PET. Cereb Cortex 2002, 12:357-368. 41. Saenz M, Buracas GT, Boynton GM: Global effects of featurebased attention in human visual cortex. Nat Neurosci 2002, 5:631-632. 42. Toth LJ, Assad JA: Dynamic coding of behaviourally relevant stimuli in parietal cortex. Nature 2002, 415:165-168. Monkeys were trained to make an eye movement in one of two opposite directions, depending on the attributes of a cue stimulus. Either the color or the location of the cue stimulus was the relevant feature throughout a block of trials. When color was relevant, the cue-response of many LIP neurons was selective for the color of the cue. However, the color selectivity was greatly reduced when location was the relevant feature. These data suggest that the encoding of stimulus attributes in parietal cortex can be a dynamic function of the task at hand. 43. Platt ML, Glimcher PW: Neural correlates of decision variables in parietal cortex. Nature 1999, 400:233-238. 44. Lauwereyns J, Takikawa Y, Kawagoe R, Kobayashi S, Koizumi M, Coe B, Sakagami M, Hikosaka O: Feature-based anticipation of cues that predict reward in monkey caudate nucleus. Neuron 2002, 33:463-473. Current Opinion in Neurobiology 2003, 13:194–197