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BRUNT. ma i ea SS" Boe Wa es oe ea Cognitive Neuroscience: Origins and Promise Michael I. Posner Seeker Fnstirne Gregory J. DiGirolamo University of Uinois at Urbana-Champaign "Both Fred and Want had boped o bate payhology onan understanding ofthe neural bai of mena vents. Their efforts were usaccessful because the suuctre and funcon ofthe human bala ws sot ‘ailabl for epic oxdy atthe piysinlogia evel Over the lt part of hs cay, thee bas been ___amming, grow and viaity In ee Bold of human brain foneion. Ie thie paer, we taco ciel ‘developments in the fields of cognitive psychology, neuropsychology, and tain gig related 10 the ‘evelopment of cognitive neuroscience. Cogtive Neuroscience has esublsed thet the decomposition ‘of mental events ca be uted with an understating ofthe mental and emotion compton cai out bythe human brain. Cogitive searosciece haste capability of iniveacing psychology in diverse seat fom how cilden develop to how adults gs rem how humans lam to how we imagine; fom. ‘oidonal coavo eo psychopatologies. Tn 1987, the James §. McDonnell Foundation held summer {ngdtue at Harvard University on cognitive neuroscience. Stephen Kosslyn was the Director of the Institute, and under his leadership, ‘an outstanding program of speakers was assembled. Michael Gaz~ ‘2aniga had persuaded John Brur, the President ofthe McDonnell "Foundation, tht it might be a good time to invest foundation funds in the creation of this new field. Michael Gazzaniga had already coined the name and had used it as the tle ofan institute that he had developed as part ofthe cogaitive science initiative stated a decade eae ‘There i a long history of investments from foundations eeating ‘now disciplines in scientific feds, For example, 2 decades ear, the Sloan Foundation invested in a number of fields, concentrating ‘in neurophysiology, and helped to create the fed of nearoscince. In terms ofthe sheer numbers of scholars altracted toa field, this venture has o be one ofthe best invesoments ever made. When the Sloan Foundation decided 0 act again to create the new field of cognitive science, they inchided psychology, linguistics and new roscienee as subdiscplines. Of course, the field of language was of major interest, and one ofthe earliest meetings in cognitive science vwas organized by Jacques Mehler (Mehler, Walker, & Garett, 1982) and was devoted slrmost entirely to this area. This meeting imzoduced European scientists to the broad range of work in cognitive tcence, At this mecting, one of us (Posner, Pea, & ‘Michael L, Rosner, Deparment of Peybiny, Seco Tense, Well Modical Ceatec, Corel Universi’ Gregory J. DiGilane, Beckman Taint, University of Winas at Urbana-Champaign. "The recench was supported in pr by Office of Naval Reseusch Geant 'N00014-96-0275 and by te Jann S. McDonnell Foundation with gaps to the Universiy of Oregon, the Weil Medea! Collegeof Comell Uni ‘esty, and the Cognitive Nowosicoce Progam and Cognitive Rehabil tation Program, CCorespondenoe concerning this nice should be adesed to Michoet 1. Porer, Saeko netae, epaceent of Psych, Box 240, 100 York ‘Aveaun, New York, Now York 10021. Eecvonic mail may be set 16 ‘mip2003@me corel ed 3 ‘Volpe, 1982) presented what was perhaps the first paper with the ‘general theme of an emerging discipline: “Cognitive Neuro- Science: Toward a Scionee of Syathesis.” Although cognitive science continues as an important enterprise, it has never hed the ‘explasive growth and influence of the ealier neurosciences inti tive. Though the sucess of afield cannot be insured by financial investment alone, a powerful scientific agenda ean attract te best ‘minds into new field and increase its chance of success ‘We think that cognitive neuroscience has just such an agenda, ‘As cognitive nesroscicnce enters the new millennium, it seems an sppropriate tie to relect on its history and to consider where the field is headed In this article, we alempt to outline some of the imtllectal background and discoveries in cognitive psychology, ‘neuropsychology, and neuroimaging that provided a foundation for the genesis of cognitive neuroscience, Because we ae not histo- flan, the treatment ie biased toward events and views that relate ‘more closely to our ovim thinking and areas of expecise: never- theless, we hope that this overview capaures the basic ideas and methods of the field, Every psychologist who entered the field in the mid-20th cen- tay studied the history of efforts to localize higher level mental fonction ia the bexin, Students ofthe fold were taught that mental function could not be localized. Karl Lashley (1925) ad discov- ered that interference with mane Jeaming in rats depended on how much tissue was removed and not on what pat of the corex wa removed, Studies of patients following traumatic frontal lobe dam. ‘age were also interpreted as showing that the brain operated as a whole during cognition. The principles of mass action and equi- potentiality were used to explain failures wo find any precise localization of cognitive function. Further, cautions were even extended to efforts to analyze cognitive processes into elements because the whole was then thought tobe differen than the sum of the parts, More specifically, it was thought that tasks were com- pletely altered when any part was changed. ‘As George Miller noted (Miller & Lenneberg, 1978), itis often ret obvious to psychologiss Why the issue of localization of function is of importance because knowing wha part of the brain | 874 | is involved may tell litle about what cognitive operations are ‘occuring. Mille (p. 6) suggested that the issue of localization is relaied to othe, moce general assumptions necessary for under- Standing the relationship between the human brain and behavior. ‘These are: 1 Complex brain functions can be decomposed into simpler, more general processes, 2. These components can be loalized anatomically and studied in elative isolation. 13. The simpler brain processes can be cortelated directly with their simpler behavior processes Inthe last several year, functional human brain imaging bas valida. many of tes sumptions. To gusp te stp and "significance of Cognitive ueuoscicace, iis impor Sreeens tetas tot sepychsigy pete wi brain imaging, that have produced this new synibesix. Table 1 ‘outlines the overall goal of using mental operations, as defined in copntive studies, to link cognition to neural systems, "We argue that development inthe understanding of localization of function and the neural excoity of the brain can influence theories and assumptions about higher cognitive processes. Spe- cifically, we review changes in the conception of major psycho- logical issues (such as priming, attention, and executive contol) ‘esulting from the growing integration of neuroscience data with cognitive data. Finally, we consider developments likely to occur fin the neae future. Cognition | Almost fiom the inception of efforts to develop models of | ‘uma cognition, investigators ft there woud be a time when cognition would be linked to developments in the brn sceaces. “esbert Simon (1981), whom many consider the founder of cog alive science, remarked ia his Compton Lectures: “The main cea forthe suembodimen: of mind 6, of cori, the teats tha Lhave just been dncusing, Te difference betwee the Icvace of @ computer and the hardware of the brain has noe ‘prevented compuers foe simulating a wide spectrum of kinds of Inoman thinking. It would be unfrtnate i this concasion were ‘teed to read that teuophysclogy has autiag to conrbu 10 ‘explanatons of human belavioe. This weold be idcalous doce. Table 1 Linking Cognitive Tasks of Daily Life to Br Level Evaple | Cogn system Language, atention, Verbal report. ‘motor contol Elementary operation Net, oa, 200m ‘Arica ineigense Pabbvay acivaton” Fact, ihibe™ Copies, ‘esl networks Neo system Pascal cone, basal PET, ERP. MBL angia Micros ‘Vint lamina rea V4 Catlular recoding Nore. framework for linking cognitive tasks of dy lite (op 20) to train systems (otlom two rows). This arcleconcenzaes on the mile ros (rows 2 and 3) by discntng how elementary inet operation ea be locallad i brain sue, PET = posiron emission tomography RP = | crencelaed poteatal, MRI = magoutie resonance imaging. ‘and tons of the human brain. POSNER AND DxGIROLAMO Iris physiology et we must tr for an explanation of the inks tf edapaton, At our koowiedge increases, the elation between posclgical and information processing explanaons will Become Jost ike the rion between quanta mechanical and physiological ‘aanations in biology. They conse wo linked levels of expx tation: the lining properdes of hefner system an showing up at the inetae been tem (p97) “The level of mutual support between these two aeas as proven ‘much closer than Simon might have suggested. [tis hoped that this article wil state both how closely Tinked the hardware ofthe brain isto the performance of cognitive and emotional tasks and. the importance of environment and self-regulation to the opera- ‘One of the iia bridge nition and brain funtion was developed by cognitive psycholo- gists in the mid-torate 1960s. Tt was demonstrated that a wide variety of tasks could be described in tems of mental operations (or subroutines) that took place over tes to hundreds of milisec- ‘nds (Newell, 1990; Sternberg, 1968) ‘The measurement of mental operations by reaction times (RTS) ‘vas always closely ssscisted with the idea of serial processing in fnoman performance. In the late 1960s, Saul Sternberg (1969) provided a general method for the isolation and investigation of ‘eral stages called the additive factors method. Tn his tsk, par- ‘icipans determined if a presented digit was a member of a set of ‘ems that they had learned previously. His data showed that successful determination generally tok place at arate of about 20 rms por item. The speed at which people could identify even complex pattems made it seem unlikely that all tasks could be ‘ought of as having the sera structure tha this task demonstrated (Treisman & Kanvisher, 1998). However, where such a scril frganizaion does apply, the additive factor: method remains powerfol tool for the analysis of mental processes and bas been applied successfully to brain imaging data (Dehaene, 1996; Saxd- et, 1998) In the mid-1980s, new developments paved the way for ¢ connection from cognitive operations (or computations) to pysi- cal architecture (or neural stucture). A numberof researchers led by Rumelhart and McClelland (1986) developed ways to analyze behavior by representing psychological concepts (eg. words) a8 a set of nodes connected by weights. This concept built on ideas of parallel dstibuted processing, for example, by representing a word as a hierarchy of features, leters, and words that were setivated in parallel, Using these methods, it was possible to simulate the empirical finding that a single Jeter bad a lower perception threshold if embedded in a word relative to being presented in isolation (Reicher, 1969) This powerful word supe- slorty effect, which appeared so counterintive in the era of purely secial meshods, was completly explicable if the stored information about words could be activated in parallel by single letters and thus reinforce the visual input to leer detectors. Cognitive. paychology proposed ways of dividing tasks into constituent operations and of using mental chronomety to mea- sure operations in empirical studies. With the advent of parallel distributed processing models, there were theoretical strvctazes i ‘which to embed the Findings of empirical studies. Now, the notion ‘of distinct cognitive modules, each computing a diferent opertion to achieve some behavior, led maturally to questions regarding localization of function. These developments provided important ‘SPECIAL ISSUE: COGNITIVE NEUROSCIENCE 875 tools to test the idea of whether these operations were localized within specific brain regions ‘With the adven: of neuroimaging it has become vecy important to document inthe milisecond range the time course of activity ia ‘neural substrates (0 distinguish purely seasory activation from top-down influences (Kosslyz, 1994), The importance of these time course measures is evidenced in proessses involved in the perception of objects (Treisman & Kanwisher, 1998). Several (pes of representation are constructed By the visual system in patallel, allowing observers to recognize, prepare actions in r= sponse to, and construct preferences toward sensory events ‘Awareness of an object is critically dependent on the frst 100 ms within 155 ms after input (DiGirolamo & Kanwisher, 1995; ‘Thorpe, ize; & Marlot, 1996). Neuroimaging and cellule studies hhave shown tht even the primary visual cortex (Posner & Gilbert, 1999) can show top-down influences; hence, a time coarse is needed to distinguish between sensory-dtiven ad attention-driven activations that appear similar in hemodynamic measures (e., Positron emission tomography [PET] or functional magnetic res ‘nance imaging (fMRI) ‘We tum to the study of neural function and localization in 2 senichronological onder of developmenc, and begin with lesion ‘methods and single-cell recordings in the next section. ‘Neuropsychology ‘he term neuropsychology has been applied to both lesion studies of mans and animals and efforts 10 record electrical activity from individual eells (or groups of cells) in higher pri rates (including some studies of human patients) The develop- rent of the microelectrode had an enormous impact on neuropsy= ‘chology. Staring inthe 1960s, the arrival of a means of exploring ‘the organization and responsiveness of the visual system of eats ‘and monkeys opeaed up new areas of exploration into the physi- ‘ology and function of brain processes (se, ¢., Hubel, 1987). In ‘the mld-19706, « number of researchers began recording cellular activity in aler-behaving monkeys (Evans, 1973; Mountcastle, Lynch, Georgopoutos, Sakata, & Acuns, 1975; Wurtz, Goldberg, & Robinson, 1980). ‘This methodology provided an important approach to understanding how the brain might cary out higher level cognitive functions like attention. Inthe following section, ‘we trace stadies of visual spatial attention from the development of ‘mental chronometry for determining the cognitive operations of spatial attention to the neural aeas involved in these operations, studies dat were based on single-cell recordings in monkeys and lesions in hurmens, Attention ‘The problem of attetion is one of the oldest in psychology (Games, 1890) and continues to be a vibrant and growing Field. The dominance of behavioral psychology in the United Stats Sn the frst half of the 20th century, however, postponed research ito the intmal mechanism of selecsive attention, Lategrty ofthe reticular formation to maintain the alert state provided anatomical reality foc one aspect (arousal) of atention (Moruzzi & Magous, 1949), The anatomical approach has led to many new Bindings relating the individ subcortical tansmiter systems (6g, dopamine, norepi- nephiine) to the computations underlying the selection of infor- ‘mation (Marroceo, Wit, & Davidson, 1994), Other approaches to attentional selection arese in work on the orienting reflex (Kal- rneman, 1973; Sokolov, 1963). However, changes inthe autonomic systems (eg, skin conductance) as a measure of orienting o°- ‘cuted over 1-2 s and made it difficult to analyze the cognitive ‘components and nevral systems underlying orieating (see, €.,, Dawson & Schell, 1982). Unlike sensory systems that can be studied in anaesthetized animals, atention requires an alet animal isteracting with the environment. Inthe mid-1970s, neurobiologits begaa to study information_processing_in_aler_monkeys_(Wurtz-et-al,1980) Because the visual system fad boon relatively well investigated sing microclectrodes, much of this work involved orienting to sual suimuli, During the past 15 years, there has been a steady ‘sdvancement i the understanding ofthe neural systems related to ‘he visual orienting of attention, Converging results have come ‘rom studies using single-cell ecording in aler monkeys (Cheluz2i & Corbeta, in press; Moter, 1998), from neuroimaging (See, 6 CCorbetta, 1998; Corbetta et a, 1998), and from lesion data (see Rafal, 1996, fora review), ‘The initial findings demonstrated a relatively restricted number ‘of neural areas in which the firing rates of neurons were selectively eahanced when monkeys were tsined to attend (0 location ot object. At te level of the superior colliculus, selective enhance. ‘ment was obtained only when the monkey also moved its eyes. i ‘contrast, neurons inthe posterior parietal lobe demonstrated solec- tive enhancement even when the animal maintained fixation. An sea ofthe thalamus, the lateral pulvinar, was similar tothe parietal lobe in containing cells that demonstrated selective enhancement Wwinenever monkeys attended (Colby, 1991). Later studies indicated ‘hat nearly ll sensory and motor systems could show the influence of attention (Moran & Desimone, 1985; Roland, 1993). Physiological scudies of cats and rodents (Skinner & Yingling, 1977) supgested that selection of the relevant chazels might Involve a thalamic gating mechanism using the reticular muleas of ‘he thalamus controlled by prefrontal sites. Peripheral gating ‘mechanisms still represent a potential source of selection that sight be especially imporant in lower rsammals. However, in ‘buman information-processing studies, twas clear that unattended {information often was processed toa high level, as evidenced by ‘an important messege on the voatended channel interfering with {he selected channel (Posner, 1978). Moce recent monkey and ‘human studies suggest that thalamic mechanisms might workin conjunction with sensory-procescing areas to gate information at cortical levels (LaBerge, 19953). The ability to sleet input chan- nels and the levels at which selection occurs has remained an active focus for cunent studies of attention. (ne effort to integrate cognitive ideas of atention with those arising in neuroscience used the ehronometvic techniques with ‘normal participants and patients who had lesions in tose axes ia ‘which atentional effects had been found in alert monkeys (Posner, (Cohen, & Rafal, 1982). To stedy how normal znd brain-damaged participants ovient, brief eves were used to provide information bout the location of a subsequent target. [n normal peticipans c ‘was found that a cue summoned attention vecy ripidly (0 its location and improved RT to targets that occurred there. If the 376 POSNER AND GIROLAMO target ocurred a an uncusd location, RTs were slowed relative the ved location ‘Once attention moved from the cued location oa new location, reorienting to the previously cued location was inhibited sith respect to other Inesions inthe visual Feld hibition of return. ‘These results semed 10 make ecological scase, in that ateation could be seen at moving tovrard a locaton of interes in advance of the eyes and was usally followed by foveaton ofthe selected IocatonInbibition of rem appeared to bea mechanism ro fvor searching in novel locations. In the 1970s, puychologisis began to distinguish between ast saaic and controlled proceses (Posner, 1978). Visual words coukd activate other words simular in meaning (semantic associates) even_ ‘when a person had no awareness of the words’ presence (Marcel, 1983), However, selecting a word meaning for active ateation appenred (0 suppress the avalabily of other word meanings. ‘Aeon was viewed less aban ery seavry botdeneck end more fsa system for providing post for motor sets, consciousness, and memory (Alport, 1980). These higher level mechauisas of attention were assumed to involve font brain areas and ‘0 provide an important meaae of coordnaing cognitive proceies. “The sesame priming suds indicated that he parallel organiza- tion found for sensory information extended to semaatc process- ing; further, both sutomatic ané voluntary processes wee involved in these higher level cogiive ubilites (Neely, 1977. ln line with this work, it was determined thet even spatial sstenton could be diferentiund on the basis of automatic or woluntary aspects. For example, fa peripheral ee indicted that thetargt would coeur elsewhere, fection was fist found athe location ofthe cue and then tthe Location indicate bythe cue It ‘ppeared that atenton could ether be summoned automaticaly by a peripheral ue or be moved voliotarly and tha the copsitive roceses involved in these operations could be isolated using hronometse methods (Posue, abot, Prieich, 8 Coben 1987) To determine ifthe cognitive operations were rlated to the sane brain acat as thse thal were modulated by alten, 1e- ‘Searcher ested patients wit esions of the pital obo thalamus, an superior coliculs on this same orienting tsk. Back paient ‘poup showed a deficit that could loosely be eae neglect ofthe convalesional side, bot the details demonstrated remurkably cif- fereat problems suggestive ofthe operations that avolved oiet- ing. Fo example, Yesions in he parca lobe primaiyprocuced deficit when aention was already engaged a different location (Gsengage) Lesions of the colialis influenced the speed of ‘movement (move), whereas thalamic lesions appeaced to make it dificult wo select target among compesiors even when station wat conectly oriented engage). Mental operations appeared lobe Tocalized in specific bran eas. However, only te presence of an interconnected vertical network of aceas (or neaal etc) could produce succesil orienting. These results suggested fea tio of opeations, one in which several brain areas all worked in concert 10 pecfom a single cognitive task. This specific model is sil in doub, and there are many ideas about how spatial ateaton ‘works. However, the idea was important in tha sugges oth that cognitive computations were anatomically localizale and that ‘most tasks involved a whole se of computations and hence, a ‘numberof separate neal areas. Exploring this idea required an ability to examine simultaneously many brain eras i normal participants while they performed cognitive tasks. However, 10 ‘method preseat inthe late 1970s could accomplish this tsk. ‘Neuroimaging ‘The effort link cognition to specific brain systems depends on having methods avaiable to secure links between cognitive com putations and neural processes (Sejaowski & Churchland, 1989) In 1978, a Scientific American ace (Lassen, Ingvar, & Skinho, 1978) reviewed the work of Seandinavian researchers exploring the use of changes in cerebral blood flow during reading. Reading 1 sory is a complex tsk and iavolves many meatal operations; during this ask much ofthe brain was ative, but te potential for ‘ure analysis was elealy present. Cognitive Anatomy Since the 1970s, under the general de of neuroimaging, many ‘methods for exploring the pars ofthe brain ative during cognitive tusks have become available (Posner & Raichle, 1994; Roland, 1993; Toga & Mezziotta, 1996). The parameters for classifying ‘methods are based on the spatial resolution and temporal precision of the techniques. PET and {MRI are two methods with good spatial solution that are used to measure bean atvity ia humane tring cognitive tasks. To move beyond the localization of ana- ‘emical areas in humans, itis useful to use methods eastive tothe time dynamics of information processing. Cognitive studies have sown that to understand cognitive operation requires analysis in ‘he millisecond range. Te temporal precision of various methods {s changing rapidly (Se, e.g, Dale & Buckner, 197), but imaging methods based on blood flow require changes in blood vessels that limit their temporal pecision to the constraints of the hemody- namic lag (~I~4 s). Eventrelated brain potentials (ERPS) and :magnetoencephalograms (MEG) are two alternative methods that hhave precise lemporal resolution. Currey, studies that combine localization methods (¢., PET) and time-dynamic methods (e4., [ERPS) provide a convenient way to ace the rapid time-dynamic ‘changes that occur i the course of humaa information processing (eee, eg, Heinze et al, 1994), Te would be ideal if noninvasive imaging methods were devel: ‘oped that provided the desized combination of high temporal and spatial resolution. However, all curent technologies have their own Timitaions. For example, celular recording is limited to snimals and is associated with sampling problems. MEG is expen- sive and, unless many channels are used, must be repositioned for examination of each ares. ERPS suffer from difficulty i localizing the neural generators of the electrical signal dretly from scalp distributions: subdermal electrode recordings solve this problem, but opportunites for such recordings are uncommon. fMRI and PET are limited by the time for blood vessels co reflect brain setvity (hemodynamic lag). Event-related (MRI uses averaging techniques sizlar to cognitive or ERP studies to improve on the time course resolution and rectifes the problem of having to block tal types (Gee, eg, D'Esposit, Zarahn, & Aguine; 1999; Jo- septs, Turner, & Friston, 1997). Bach ofthe extant methods will lead to modifications that may address some or all of these prob- lems, and new methods are becoming available all he time (se, eg, Gratton & Febiani, 1998). SPECIAL ISSUE: COONTTIVE NEUROSCIENCE 87 Experimenial design. A frequent design for brain imaging studies involves a comperison of an experimental condition with a control condition. In PET, for example, one often subtracts the dara ‘blained in the contol condition from the experimental condition, ‘with the goal of determining what operations are uniquely in- volved in the experimental condition. Consider an effort «0 see ‘what pans of the brain sre involved in sensing motion. If the ‘experimental condition is a set of moving dots and the control condition is the same dots without motion, a subtraction may be ‘thought to involve motion sensitive areas (Zeki, 1993). This type ‘of design has been quite successful in localizing areas of th visual system that ae related 10 processing motion, color, or form. A quite different design. js to use the same stimuli but require the ‘participant o atid wo different aspects ofthe stimuli, Attention to ‘motion in one condition versus altending to colar or form in another condition bas been shown to activate prety much the same areas as when subtracting activation from moving versus nonmoy- ing stimuli (Coretta, Miezin, Dobmeyer, Shulman, & Petersen, 1990) Things become more complicated when higher level cognitive processes are involved, Ibis certainly not possible to say that most experimental and contro tasks differ in only one way. For exam pile, consider a tas in Which one wishes to undeestand how a word association is generated; the experimental condition may involve ‘generating the use of a noun (e.g. see hammer and say "pound"), ‘whereas the contol condition miay involve merely reading the ‘word aloud. "The resulting subtraction might cid one of the sensory and motor components but leave intsct a number of operations related to differences in atention and effort required between the experimental and control tsk, as well as de operation of fterest (Gc, Semantic processing). This issue has sometimes been called the problem of pure insertion, and it is generally agreed that it is ‘pot posible to guarantee successful contol of all but one operation. Fortunately, the isolation of cognitive operations ean be achieved in differeat ways for imaging studies than for pucely ‘ehavioral methods. Table 2 indicates the use of a hierarchical nandbook (pp. 381-605). Boston: Bikaner Bourke, P. A, Duncan, J, & Nimmo-Smith 1. (1996). A general factor Involved daslask performance daseineet, Quarterly Journal of ‘Seperimenal Pochology, A, 505-545. 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