The Behavior Analyst 2002, 25, 161-173 No. 2 (Fall) from a Behavioral Perspective: A Critique of Chasing Ghosts with Geiger Counters Steven F Faux Drake University

Cognitive neuroscience is a growing new discipline concerned with relating complex behavior to neuroanatomy. Relatively new advances in the imaging of brain function, such as positron emission tomography (PET), have generated hundreds of studies that have demonstrated a number of inter- esting but also potentially problematic brain-behavior relations. For example, cognitive neurosci- entists largely favor interpretations of their data that rely on unobserved hypothetical mechanisms. Their reports often contain phraseology such as central executive, willed action, and mental imagery. As B. F. Skinner argued for , cognitive constructs of neurological data may yield nothing more than a conceptual nervous system. Key words: cognitive neuroscience, PET, fMRI, ERP, brain imaging

During the 50 , cognitive 2001). Further, many in cognitive neu- scientists have transformed their field roscience attempt to give a brain lo- by embracing a variety of different dis- cation to those unobserved processes ciplines and subdisciplines (Gardner, using gross measures of physiology 1985; Solso, 2001). For example, they (e.g., Roland, 1993). have made use of various versions of This paper will update an argument linguistics (e.g., Chomsky, 1959), phi- originally made by Skinner (e.g., 1938/ losophy (e.g., Fodor, 1975), symbolic 1991, 1950, 1953, 1974) that super- logic (e.g., Newell & Simon, 1976), imposing unobserved mechanisms and connectionist architectures (e.g., upon the brain results in little more Grossberg, 1988). This paper is a cri- than a "conceptual nervous system," tique of certain practices that charac- with a great potential to misguide (see terize a popular new version of cogni- also Uttal, 2001). Much of cognitive tive called cognitive neurosci- neuroscience still relies on mentalistic ence. Its growing popularity is due, in forms of explanation that either explic- part, to its use of sophisticated brain- itly or implicitly appeal to an inner imaging technology involving positron agent, "the ghost in the machine," in emissions, magnetic resonance, and the words of Ryle (1949). Although the brain-electric fields. However, cogni- technology of cognitive neuroscience tive neuroscience has not improved is impressive (e.g., tracking gamma ra- upon the assumptions found in older diation in the brain), it is the opinion cognitive . It often assumes of this author that those measurements that reasonable inferences about unob- amount to little more than chasing served neural mechanisms can be ghosts with Geiger counters. This pa- made from overt behavior (see Uttal, per argues that much of cognitive neu- roscience is mere conceptual neurology I thank W. Scott Wood of Drake University that tends to obscure rather than further for helping me formulate the ideas in this paper scientific progress. It will also address and for comments and reactions to an earlier a number of methodological concerns. draft. A version of this paper was presented at the 27th annual meeting of the Association for Behavior Analysis, May 26, 2001, New Orleans. A BRIEF OF Address correspondence to Steven F Faux, COGNITIVE NEUROSCIENCE Department of Psychology, Drake University, Des Moines, Iowa 50311 (e-mail: steven.faux@ Cognitive neuroscience emerged as drake.edu). a new discipline when cognitive sci- 161 162 STEVEN F. FAUX

Major Dependent Variables in Journal of Neuroscience 80 Cognitive ~0 en 60 U~~~~~~~~~~~~~~~~~ '- Q) 0 ' °-O = behavioral Irt, error rates, etc.) a 20 0) | = functional (ERP/PET/fMRI) L. 0) 0 0

1988 1991 1993 1995 1997 1999 2001 Figure 1. Percentage of empirical articles in each volume of the Journal of Cognitive Neuroscience using either traditional behavioral measures (e.g., reaction , error rates, etc.) or brain-imaging measures (PET, fMRI, or ERP) in the past 10 years. entists began combining their old cog- at its inception and by its 12th volume nitive-perceptual paradigms with the publishing well over 1,000 pages per new brain-imaging procedures (Servos, year. Citations of cognitive neurosci- 2000). The most important brain-im- ence studies now appear widely in aging technologies that have shaped common textbooks of undergraduate the field are positron emission scan- (e.g., Solso, ning (PET), functional magnetic reso- 2001; Willingham, 2001) and introduc- nance imaging (fMRI), and -re- tory psychology (Kosslyn & Rosen- lated potentials (ERPs). These technol- berg, 2001; Myers, 2001). ogies (described in more detail below) In the past, cognitive science has re- give some measure of brain activity lied largely upon reaction time as its with varying degrees of temporal and primary dependent variable. Reaction spatial resolution. were used as an indirect measure In 1988, the Journal of Cognitive of mental , that is, the Neuroscience began publication, and speed of mental processes (e.g., Posner, shortly thereafter, the Cognitive Neu- 1986). Although reaction time is still roscience Society (with the acronym important, cognitive neuroscience has CNS) was founded in 1994. CNS be- added three brain-imaging technolo- gan with a membership of about 400 gies (PET, fMRI, and ERP) to its ar- and is now about 2,000 and growing mament. Tabulation of dependent var- (Tara Miller, personal communication, iables used in all empirical articles in 2001). The Journal of Cognitive Neu- the Journal of Cognitive Neuroscience roscience is a peer-reviewed quarterly. between 1991 and 2000 (see Figure 1) Its empirical articles are on standard shows an increasing reliance on brain- topics of cognitive science, which in- imaging techniques relative to tradi- clude working , verbal perfor- tional behavioral measures in cognitive mance, visual , and mental psychology. Cognitive neuroscience imagery. The journal has grown steadi- has become a brain-imaging science. ly, publishing about 300 pages per year It is easy to understand why some COGNITIVE NEUROSCIENCE 163 scientists, editors, and readers would ity may be several millimeters in any be attracted to this imaging technology. direction. PET brain activity is often The imaging instruments themselves measured while the participant contin- are the result of advances in atomic uously engages in some behavioral physics, electromagnetism, and micro- task (e.g., reading a list of concrete computers. Images from functional nouns presented one at a time or lis- brain scans are often color coded (like tening for a target tone that requires a weather maps) and produce spectacular button press). Multiple stimuli (trials) color plates in journals. The data ap- usually are presented over the time it pear to take the reader a step closer to takes to make a single PET scan. Be- the "black box" of brain operations. cause of the temporal constraints, there Hence, a brief description of the three is little or no ability to resolve PET ac- most widely used imaging techniques tivity as a function of trials or stimulus is useful and is given below. presentations within a task. A typical experiment requires six to ten scans THE IMAGING TECHNOLOGY made about 10 min apart (Cabeza & AND DEPENDENT VARIABLES Nyberg, 1997, p. 3). Scans from an in- dividual participant are averaged, and Positron Emission Tomography then data from multiple participants are This technique is essentially a com- grouped to create grand averages. puterized Geiger counter that can iden- tify regions of radioactivity in the Functional Magnetic Resonance brain. Human participants are admin- Imaging istered (by inhaling or by injection) ra- dioactive isotopes, such as oxygen-15, Functional MRI is similar to PET in nitrogen-13, or carbon-Il, that can be that it provides a measure of blood absorbed by the brain. Brain regions flow-in this case, localized blood ox- presumably activated during a cogni- ygen (see David, Blamire, & Breiter, tive task selectively absorb the isotopes 1994, for introductory review). How- and become differentially radioactive ever, it differs in that no radioactive for a short time (see Cabeza & Nyberg, substances are involved. This tech- 1997, 2000; Roland, 1993). nique utilizes magnetic fields (having a Depending upon the protocol, PET magnetic strength of about 2 to 4 Tes- can measure regional variations in la) and the magnetic properties of he- blood flow, blood volume, oxygen con- moglobin to produce functional brain sumption, and glucose utilization, images. Because deoxyhemoglobin is among others (Raichle, 1996, p. 190). more magnetic than oxygenated he- Oxygen-15-labeled water with a half- moglobin and surrounding tissue, the life of 123 s is the substance most often fMRI machine is able to detect differ- used in PET studies (G. I. Shulman et ences in oxygen levels. This technique al., 1997, p. 642). As neurons become is called blood-oxygen-level-depen- active, the labeled water is locally con- dent (BOLD) fMRI. sumed during oxidative metabolism, Although fMRI images can be made creating differential regions of radio- quickly, it takes 3 to 6 s for oxygen to activity in the brain (Roland, 1993). concentrate in brain regions that be- PET scan measures of gamma radi- come neurologically active (Servos, ation are converted to estimates of re- 2000), creating a functional limit to gional cerebral blood flow. The typical scanning rate. An fMRI machine usu- scan takes about 40 to 70 s, with a spa- ally scans about every 2 s with a res- tial resolution of between 6 and 15 olution of about 2 mm. Special proto- mm. This means that a single PET im- cols sometimes allow multiple scans represents a summary of brain ac- per . These specifications are tivity over a period of about 1 min, and significant improvements over PET. that the error in localizing brain activ- However, both fMRI and PET use ex- 164 STEVEN F. FAUX perimental methods that are nearly A PROTOTYPICAL PET identical. STUDY WITH A BRIEF CRITIQUE Event-Related Potentials To illustrate problems of interpreta- ERPs are averaged brain electrical tion and method, a particular PET scan responses (EEG) recorded from the study (Mellet, Tzourio, Denis, & Ma- scalp and time locked to specific stim- zoyer, 1995) will be described in detail. ulus presentations (see Coles, Gratton, This study has been chosen because it & Fabiani, 1990, for introductory re- is fairly typical of the experiments in view). Typically, the recording this field. Its results are cited in re- (i.e., ) is about 1 s beginning spected textbooks (e.g., Richardson, with the onset of the stimulus. ERPs, 1999, not only cites this study in detail also called averaged evoked potentials, but uses color plates from this study on are the average brain response of its cover), and it is one of the rare re- somewhere between 30 and 1,000 ports that actually provides some in- stimulus presentations depending on dividual-participant data, an issue im- the signal-to-noise ratio of the back- portant to behavior analysis. ground EEG. Eight individuals participated in ERPs demonstrate that brief stimu- three behavioral conditions; PET mea- lus presentations evoke morphological- surements were made for an 80-s du- ly specific electrical responses from the ration in each condition. The first con- brain. Early potentials, within the first dition, a baseline, consisted of making 200 ms, are to reflect the neu- a PET scan while the volunteer was re- ral volley passing from synaptic junc- laxed with eyes closed. The second, a tion to synaptic junction. The neural perception condition, consisted of tak- sources of later evoked responses be- ing a scan while the participant viewed yond 200 ms, termed long-latency po- a cartoon map of an island with various tentials, are less easily identified. The landmarks along its perimeter (huts, tendency in the literature has been to trees, wells, mountains, etc.). Partici- link early ERP responses to primitive pants were instructed to move their sensory systems and long-latency eyes systematically clockwise from ERPs to complex cognitive-perceptual landmark to landmark on the island, systems. The functional role of the and then to move eyes counterclock- ERP in the brain, if any, is not known. wise. The third condition involved The peaks and valleys of any given mental imagery. With eyes closed as in brain potential probably have multiple the baseline condition, the participants neural generators with complex inter- were scanned while they mentally vi- actions that are nearly impossible to sualized the map and moved their eyes tease apart (see Coles et al., 1990, as if viewing the landmarks of the map. chap. 13; Donchin & Coles, 1988). The From previous work (i.e., Kosslyn et most prominent long-latency potentials al., 1993), Mellet et al. (1995) expect- in the cognitive neuroscience literature ed to find activation of the primary and are the produced by task-relevant association visual cortices in the im- discriminative stimuli (reviewed in agery condition relative to baseline. Donchin & Coles, 1988), and the Mellet et al. presented regional cere- N400, produced by contextually irrel- bral blood flow (rCBF) results for all 8 evant verbal stimuli (reviewed in Kutas individuals from six brain regions in & Van Petten, 1988). both left and right hemispheres (see the The remainder of the paper will con- histograms in Figure 4 of their report). centrate on PET findings. However, Positive rCBF values indicated brain with few exceptions, the problems activation (increased blood flow), and raised for PET apply in some form to negative values indicated deactivation fMRI and ERP. (decreased blood flow) relative to base- COGNITIVE NEUROSCIENCE 165

line. In the "perception minus base- perature map. However, on a PET line" data, activation of primary visual brain image, hot colors (reds and yel- cortex and superior occipital cortex lows) represent regions of relatively was observed to be positive, relatively high radiation and cool colors (greens large, and consistent across all 8 par- and blues) represent regions of rela- ticipants. In addition, relatively consis- tively low radiation. Although the Mel- tent positive responses were found in let et al. PET scan graph of Subject 8 superior parietal and precuneus areas. in the imaging condition showed the So far, the interpretation is clear- existence of many red hot areas in su- looking at something activates visual perior occipital cortex, the same data areas of the brain. Less well explained presented in histogram form for that in the Mellet et al. report is that con- participant reveal that actually very sistent deactivation was observed in small rCBF values were coded as red superior temporal cortex and the infe- hot. In fact, little rCBF variation was rior frontal region. A consistent prob- observed in other brain regions for this lem with any cognitive interpretation participant, suggesting the color scale of PET data is determining why certain (going from hot red to cool blue) rep- brain regions are activated while others resented an extremely small range of are deactivated. This issue will be elab- numeric values. (Perceptually signifi- orated below (see Additional Problems cant color differences in PET scan with PET). graphs do not necessarily equal physi- In the "imagery minus baseline" ologically important differences.) For data, what was most striking was the most other participants the rCBF val- strong variability across participants. ues in superior occipital cortex (as in- The primary visual cortex showed dicated by histogram) were dwarfed by rCBF values with large fluctuations go- values found in other brain regions. ing in both positive and negative direc- Thus, if all participant data were pre- tions depending on the participant. The sented in color image form, no consis- superior occipital cortex data showed a tent patterns of anatomical activation little more consistency but with very would be evident. In other words, the weak values generally in the direction red hot regions would be quite differ- of activation (increased blood flow). ent for each individual. This lack of All other brain regions showed fairly consistency across individuals blurs strong variability. any useful scientific interpretation. Despite variability among partici- Despite large individual variability, pants, Mellet et al. (1995) should be the authors concluded that mental im- commended for publishing a full-color agery is associated with activation of plate of a PET scan identified as "Sub- the superior occipital cortex. Mellet et ject 8" (see their Figure 5). Systematic al. (1995) used their data to support the presentation of individual data is rarely idea that the visual association cortex done in the field. This brain scan creates mental images or "stored rep- showed the superior occipital cortex resentations common to visual percep- lighting up with hot-colored values tion, and a similarity of processes that (reds and yellows in the original plate) access and manipulate these represen- in the mental imaging condition, indi- tations" (p. 433). In fact, the data and cating that rCBF values were the larg- the conclusions are not terribly persua- est in this region relative to all other sive, because the behavior of mental brain regions. (This is the result that imaging appears to produce no consis- Mellet et al. had predicted.) Unfortu- tent topographic relations across indi- nately, these results do not represent viduals. the full story. Such color-coded data Linking mental imagery with PET is have the potential to mislead unless not just a process inferred, but is a pro- carefully analyzed. Colors on a PET cess "deferred." As Skinner (1974) ar- scan are similar to the colors on a tem- gued, "An inner copy makes no prog- 166 STEVEN F. FAUX ress whatsoever in explaining ... [the] subjects of all scans. Find brain regions physiology of perception" (p. 81). He with averages that are statistically dif- goes on to say, "It is as difficult to ex- ferent from zero. plain how we see a picture in the oc- 5. Conclude that statistically signif- cipital cortex of the brain as to explain icant brain regions account for cogni- how we see the outside world, which tive process, P. it is said to represent" (p. 81). Map Three main critiques of the subtrac- reading is not an ability that needs to tion method are provided, and each re- be conferred on neurons. The ghost is volves around the cognitive constructs not in the machine. It is just a machine. themselves. This paper is not intended to be a general statement against the study of Criticism 1: Cognitive Atoms brain-behavior relations. Instead, this Have Not Been Identified is a proposal that science progresses best when physical brain measure- Because any given cognitive process ments are tied to overt behaviors. As is based on inference, it seems impos- Skinner (1938/1991) stated, "Before sible that a treatment task could ever ... [a neurological] fact may be shown be designed so that it differs from a to account for a fact of behavior, both baseline task by only a single brain op- must be quantitatively described and eration (cf. Sergent, 1994). To their shown to correspond in all their prop- credit, cognitive psychologists have erties" (p. 422). Mental imaging as an recognized this issue and have even inferred behavior has not been ade- given it a name-the pure insertion quately quantified to meet the above problem (Sartori & Umilta, 2000). As criterion. an example, a recent cognitive neuro- science study of reading comprehen- EXPERIMENTAL DESIGN: sion notes, "Even simple tasks, hy- THE SUBTRACTION METHOD pothesized to index selectively partic- ular aspects of language processing, of- This critique of practices within cog- ten do not tap only one component of nitive neuroscience requires some un- language processing but encompass a derstanding of the most widely used complex chain of processing" (Bave- experimental design in the field: the lier et al., 1997, p. 666). This statement subtraction procedure. It is the standard does not go far enough. The claim that design of PET and fMRI studies a given behavior differs from another (Raichle, 1996), and variants of the de- behavior by a single cognitive process sign are often found in ERP studies. is nothing more than a best guess. The The subtraction method, involves the word single is an uninformative mod- following steps (elaborating on Smith, ifier of an inherently ill-defined con- 1997): cept. Because cognitive operations 1. Identify some treatment task that cannot be directly observed, subcom- involves the cognitive process, P. ponents of an operation cannot be dis- 2. Identify some baseline task that is sected or disentangled, let alone count- identical to the treatment task but does ed. not involve cognitive process, P. Cognitive neuroscientists often 3. Collect separate brain scans dur- make arguments as if everyone has ac- ing the baseline and treatment tasks. cepted a periodic table of cognitive at- Repeat scanning several times within oms known to make up cognitive com- subjects and tasks. Compute an aver- pounds. For example, Smith (1997) ar- age scan for each individual within gues that "you can end up drawing the each task. wrong conclusion, if the concept you 4. Subtract average baseline scan re- are attempting to localize [in the brain] sults from average treatment scan re- is itself readily decomposable into sults. Compute a grand average across more primitive cognitive concepts" (p. COGNITIVE NEUROSCIENCE 167

168). It is difficult to conceptualize a changes in activation, involving per- primitive cognitive construct, particu- haps millions of neurons. Brain scans larly because no criteria are given. This can and do miss smaller regions of ac- problem of primitivism is made evi- tivation (e.g., Fitzpatrick & Rothman, dent by Smith's own attempt to explain 1999, review some current controver- unexpected results in a spatial working sies in neuroenergetics). Neurological memory task. He states, "Spatial significance is not necessarily that working memory can be decomposed which is "large." Further, PET and into a pure storage component (a spa- fMRI are not direct measures of neural tial buffer) and a rehearsal component, activity, only blood flow. It is an as- ... the latter involv[ing] selective at- sumption that momentary regional tention" (p. 168). First, it is not likely blood flow (a slow process of several that there would be much agreement after a stimulus; see Servos, on this particular decomposition of 2000) reflects the most relevant neural spatial working memory (cf. Johnston regions of a behavior. & Dark, 1986). Second, one must won- It is a little frightening when one der how useful it is to break one vague strings together the assumptions made construct into three vague constructs. in PET studies. PET investigators as- In a sense, however, Smith is correct. sume that increased gamma radiation If relevant variables are not under indexes increased cerebral blood flow, proper experimental control, then the which presumably indexes neural ac- results are likely to be uninformative tivity, which presumably indexes cog- or misleading. nitive processing. Skinner (1950) might as well have been addressing Criticism 2: Vague Cognitive Labels PET assumptions when he criticized Do Not Elucidate Vague Anatomy mental and physiological theories for being based on "events taking place Cognitive neuroscientists have failed somewhere else, at some other level of to justify why unobserved cognitive observation, described in different constructs make useful labels for par- terms, and measured, if at all, in dif- ticular brain regions. PET and fMRI ferent dimensions" (p. 193). reports assume that different images Servos (2000) argues that cognitive between the treatment task and base- cataloging of cortical anatomy is an line task reveal anatomical locations important scientific step, even if it is important to the production of some not much different than "stamp col- . However, it is more likely lecting" (p. 72). However, there are that PET or fMRI changes exist, not reasons to disagree. In cognitive neu- because a single cognitive process has roscience the cognitive events to be been segregated, but because treatment classified are obscure, unlike stamps. and baseline simply involve different And, although brain regions can be ob- behaviors. served and defined in gross terms, the Uttal (2001), from another behavior- underlying circuits that mediate cog- al perspective, has described cognitive nition cannot. It is doubtful that sci- neuroscience as the "new phrenolo- ence can progress by making gross gy." At best, PET and fMRI measure- physiological measurements to support ments take us from not knowing what ill-defined cognitive constructs. is happening in the whole brain to not Level of resolution is still not the knowing what is happening in some root of the problem. Use of cognitive particular gyrus. It is tempting to coun- metaphors cause miscommunication ter that "this is progress," but there are even when studies are conducted at the reasons to believe that this form of cellular level. For example, Shadlen brain reductionism is inappropriate. and Newsome (1996) studied the firing For example, brain-imaging procedures of nerve cells in the lateral intraparietal are sensitive only to large regional cortex and showed that some cell ac- 168 STEVEN F. FAUX tivity was correlated with the difficulty HOMUNCULUS RESURRECTED: of perceptual decisions. Such cells THE CENTRAL EXECUTIVE were coined decision cells. Provoked by this terminology, a news feature in Dennett (1991) has argued that a a recent issue of Nature concluded pervasive flaw of cognitive neurosci- "Decision cells could form the basis ence models is that they "still presup- for a 'central executive' in the brain" pose that somewhere, conveniently hidden in the obscure 'center' of the (Kast, 2001, p. 127). The effectiveness mind/brain, there is a Cartesian The- of a science must be judged by the pre- ater, a place where 'it all comes to- cision of its terminology. gether' and consciousness happens" (p. 39). Sadly, one does not have to Criticism 3: The "Cognitive" in look far to find a neurological discus- Cognitive Neuroscience Is Not Tested sion of the "central executive" (e.g., Baddeley, 1995; Collette et al., 1999), In the subtraction method, as Smith ".willed action" (e.g., Badgaiyan, (1997) has recognized, "no matter 2000; Frith, Friston, Liddle, & Frac- what appears in the [treatment minus kowiak, 1991), or "supervisory atten- baseline] difference image" (p. 167), tional systems" (e.g., Bayliss & Rood- some proposed cognitive processes can enrys, 2000; Shallice, 1991). In a re- be said to be responsible for that dif- cent review article published in Psy- ference. Thus, cognitive constructs are chological Bulletin and titled not directly tested in the subtraction "Cognitive Neuroscience: Origins and method, because no brain-imaging re- Promise," Posner and DiGirolamo sult could ever refute a cognitive the- (2000) state, "We believe ... ory. Instead, cognitive constructs are and volition are at the very heart of the only "mapped." True, brain maps may psychological enterprise" (p. 885). be revised from study to study, but the Yet, attention and volition are vague cognitive constructs themselves have a concepts that could be inferred from al- status that is relatively immune to ex- most any behavior other than sleeping. perimental revision. How can such broad concepts be at the The correlation of so-called cogni- heart of a scientific enterprise? Scien- tific terminology without behavioral tion with brain activity is inevitable. precision is at risk of being useless re- Why inevitable? Because for any given ification. behavior, X, there will always exist One of the most popular metaphors some unobserved cognitive explana- of cognitive neuroscience is the central tion, Y. Once X is legitimately tied to executive, a mechanism that is often a brain measurement, there is little to viewed as being independent of the hinder Y from being tied to the brain senses, providing output without input as well. (see, e.g., Kast, 2001). The cognitive In the whole enterprise, there is no literature often locates the central ex- indication of how one can go from ecutive in the frontal lobe (Gazzaniga, brain maps to controlling or manipu- Ivry, & Mangun, 1998). For example, lating behavioral or neurological vari- Marshuetz, Smith, Jonides, DeGutis, ables. The goal of the research pro- and Chenevert (2000) cite literature to gram appears to be to map and label argue that "the ventrolateral and dor- the brain. One cannot object to map- solateral prefrontal cortex ... are ping or even labeling parts of the brain thought to mediate executive process- as being associated with specific be- es" (p. 130). They then define the ex- havioral functions. However, there is ecutive processes. Again, to quote no good reason to make cognitive ter- Marshuetz et al. (2000): "Among [the minology the de facto language of the executive processes] are attention-and- neuroscience of complex behavior. inhibition ..., task management COGNITIVE NEUROSCIENCE 169 monitoring ..., and coding ... in Frith et al. found that the treatment memory" (p. 13 1). How can neuro- condition minus the baseline condition anatomy clarify the issue of task man- showed increased activity in the dor- agement, coding, and memory as ex- solateral prefrontal cortex with some ecutive processes? How would one involvement of the anterior cingulate recognize the operations of an execu- cortex. Their primary interpretation tive in terms of physiology? These was that the frontal cortex has a sig- questions are seldom addressed. A be- nificant role in willed action. havioral perspective suggests that le- One must wonder what behaviors gitimate brain-behavior relations be- would and would not be considered come trivialized when tied to a meta- "willed actions." It is hard to imagine phorical central executive. reasonable definitional criteria. A lack The problem of vague terminology of stimulus control in an experiment is illustrated in a widely cited PET does not result in "willed" behaviors; study of willed action, considered by it merely results in behaviors not under some cognitive neuroscientists to be a the control of the experimenter. Frith et classic in the field (e.g., Gazzaniga et al. (1991) are probably not suggesting al., 1998; R. G. Shulman, 1996). The that complex behaviors are unlawful, report is by Frith et al. (1991) titled but if they are not making that sugges- "Willed Action and the Prefrontal Cor- tion, then a much better terminology is tex in Man." Six volunteers in each of needed. two studies inhaled oxygen-15-labeled What kind of empirical data would carbon dioxide while they performed challenge Frith et al.'s (1991) results simple tasks for 3 min. In one study and interpretation? R. G. Shulman the tasks were verbal in nature, and in (1996) struggled with this question af- the other the tasks were somatosenso- ter having tried to replicate their results ry. The baseline task in the verbal using fMRI. His laboratory found cor- study consisted of repeating common relations in slightly different brain re- words presented by the experimenter, gions. In a candid and bold interview such as man or hot. The treatment task with the Journal of Cognitive Neuro- required the volunteers to generate science in 1996, Shulman argued that words beginning with the letter F, such the use of cognitive concepts in neu- as fox or first, as the experimenter roscience has interfered with under- prompted each response by saying standing brain activity. He argued, "next." The baseline task in the so- moreover, that PET and fMRI data matosensory condition consisted of "when examined more critically are volunteers moving the same finger not really telling us much about how touched randomly by the experimenter. the brain enables cognition" (p. 475). The treatment task consisted of moving Referring to constructs such as willed any finger of choice (avoiding repeti- action, attention, and working memory, tion) when prompted by a touch on a Shulman said, "Given the primitive finger. state of cognitive concepts and the According to Frith et al. (1991) both strengths of functional imaging baseline tasks involved volunteers giv- this is the time for revising concepts in ing an exact response to a stimulus, response to ... the experiments, rather whereas both treatment tasks involved than asking experiments to subserve making a choice from a population of the concepts" (p. 476). No behaviorist potential responses. By their interpre- could supply stronger testimony. In- tation, the primary differences between deed, neuroscience has made consid- the baseline and treatment tasks were erable strides in tying observable be- willed action or internal response gen- haviors to specific brain locales (see, eration-defined as novel behaviors e.g., Kandel, Schwartz, & Jessell, not specified by a stimulus. In both 2000, for current reviews). By contrast, modalities, verbal and somatosensory, there is no strong evidence that in- 170 STEVEN F. FAUX ferred mental operations have clarified With the inherent ambiguities of posi- neurophysiology. tive and negative values in PET data, one can appreciate why Frith et al. ADDITIONAL (1991), summarized above, might puz- PROBLEMS WITH PET zle over the following: "In both [our] studies, decreases [italics added] were Cognitive constructs are not the only observed in cortical areas concerned source of ambiguity in PET. The PET with the modalities specific to the datum itself is inherently difficult to in- study" (p. 245). Specifically, Frith et terpret. al., in a word-generation study, found decreased activity in the left superior Distinguishing Activation temporal cortex (a language-related re- from Deactivation gion), and, in a somatosensory study, The PET concepts of activation and found decreased activity in the sensori- deactivation are sometimes miscon- motor (pre- and postcentral) cortex. strued as being related to neural exci- These findings, however, were glossed tation and inhibition. In fact, these PET over because both studies found acti- terms have no clear relation to under- vation in the frontal lobe. Apparently, lying neural behavior. Perhaps without only the frontal lobes showed enough justification, the PET literature has rou- of the "central executive" character- tinely emphasized behavioral correla- istic of being "active" at a consistent tions with activation over those with location "where it all comes together." deactivation (reviewed by Cabeza & Nyberg, 1997, 2000). However, PET The Problem of Intrinsic activation and deactivation have little Variability and Averaging to do with a neuron's firing threshold. Activated and deactivated brain re- Attempts to manipulate variability in gions are determined statistically rela- brain-imaging experiments have not tive to some baseline, and reflect been made at the individual level. Typ- changes in blood flow and metabolism. ically, data are grouped and individual Specifically, brain activation refers to variability is obscured. The cognitive an increase in localized blood flow, neuroscience approach appears to ac- and deactivation refers to a decrease. cept that large variation is intrinsic to Although excited neurons would typi- the operations of the brain, and that ex- cally expend more energy than inhib- perimental control of individual varia- ited ones, neurons that produce inhib- tion is not possible. As Sidman (1960) itory postsynaptic potentials do expend has argued, "Acceptance of variability metabolic resources, and large groups as unavoidable or, in some sense, as of such neurons could show up as "ac- representative of the 'real world' is a tive" on a PET scan (Kandel et al., philosophy that leads to the ignoring of 2000; Roland, 1993). Moreover, excit- relevant factors" (p. 152). Unfortu- ed neurons are often closely surround- nately, in most PET, fMRI, and ERP ed by inhibited (hyperpolarized) neu- studies total variability is mostly swept rons (Roland, 1993). "Deactivated" under the rug. Multiple brain-imaging neither means inhibited nor behavior- measurements over time are averaged ally unimportant. So-called deactivated (a process called signal averaging) regions could still have considerable within an individual to determine the neural activity and therefore could be presence or absence of a neural re- a neural source for any given behavior. sponse. Individual averages are then For these reasons, designated regions grouped to create grand averages. In- of PET activation are ambiguous with dividual results are rarely displayed, respect to the behavior of neurons. and brain maps are never displayed Regions of activation or deactivation with error bars. Both intraindividual cannot be predicted with any precision. differences and interindividual differ- COGNITIVE NEUROSCIENCE 171 ences are obscured (Raichle, 1996, p. studies even when similar tasks were 191). With so much variation, it is rea- used. For example, five of the "atten- sonable to ask how well averages ac- tion" studies used comparable versions count for individual results. This ques- of the famous Stroop task involving tion has not been addressed. color naming (see Table 1 in Cabeza & Nyberg). Totaling over the five studies, The Problem of Statistical Tests 20 regions of brain activation were found to be related to the Stroop task. This is not the place for a detailed Two studies showed Stroop-related statistical critique. However, in PET brain activation predominantly in the and fMRI, thousands of measurements left hemisphere, two showed activation make up a single brain image. Further, predominantly in the right, and one a single brain scan will produce mul- showed bilateral activation. No single tiple brain slices several millimeters region of brain activation was common apart. Standard multivariate statistics to all five studies. Three of the studies are not possible because there are agreed on the involvement of Brod- many more measurements than there mann area 32 on the left, and another are participants. However, some data- two agreed on Brodmann area 40 on reduction techniques have attempted to the left. The striking finding was not solve this problem (see, e.g., Almeida the agreement but the disproportionate & Ledberg, 2002; Fletcher et al., amount of disagreement (see Tables 1 1996). Typically, studies use univariate through 8 in Cabeza & Nyberg). Ca- statistical tests on each of the thou- beza and Nyberg admit that PET re- sands of voxels (pixels) in a PET im- sults are "determined to a high degree age. Not only does Type I error inflate by both the particular target and ref- due to multiple correlated tests, but sta- erence tasks employed" (p. 21). Fur- tistical significance, accurate or not, ther, vague cognitive constructs tied to may have little direct relation to neu- flawed experimental designs produce rological significance. little reliability. The Problem of Replication CONCLUSION Given the kinds of problems out- lined here, there should be no surprise Cognitive neuroscience is gaining in that replication is a difficult proposi- popularity because of its attempt to lo- tion in many brain-imaging studies of calize traditional cognitive constructs cognitive neuroscience. Rare is inter- in neuroanatomy. However, too many group replication, quite rare is intra- proposed cognitive mechanisms are subject replication, and intersubject vague, unnecessarily complex, prema- replication is extremely rare (see Ca- ture, and amount to little more than in- beza & Nyberg, 1997, 2000, for re- ferred guesswork. Unobservable be- views). haviors of the mind, like volition, cen- The problem of replication cannot tral executive function, and mental im- be thoroughly reviewed here, but the agery, do not enhance understanding of reader is referred to Cabeza and Ny- empirical brain operations. In fact, berg (1997) for an extensive review of such terminology obscures more than 73 PET studies with tabular summaries clarifies. Significant problems exist of each study. Sixteen of those studies with the standard experimental para- were categorized under the topic of at- digm, the subtraction method. For ex- tention, even though most studies used ample, cognitive constructs are not very different behavioral tasks. Even tested in the subtraction method, and so, they concluded that attention "gen- brain images are incapable of refuting erally engages frontal and parietal cor- traditional theories of cognition. In- tices" (p. 21). More striking, however, stead, cognitive constructs are being is the variability of findings among used as labels to name the proposed 172 STEVEN F. FAUX functions of the cortex. Cognitive neu- (pp. 413-455). Cambridge, England: Cambridge University Press. roscience theories cannot predict im- Collette, F, Salmon, E., Van der Linden, M., portant variations in data, such as when Chicherio, C., Belleville, S., Degueldre, C., et activation and deactivation should be al. (1999). Regional brain activity during found. Brain maps add little to science tasks devoted to the central executive of work- if they provide little more than vague ing memory. 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