Abstract

Receiving the National Academy of Neuropsychology's Lifetime Contributions to Neuropsychology Award promoted reflection on values and decisions. Selecting the topic of the presentation associated with the award also led to rumination. The term “lifetime” was the deciding factor: how does one choose and start a career path, what advice might one give to individuals embarking on their own career, and what goals does one set up early in one's career? What are the “drivers” in one's life? This was the topic of my presentation, and the theme of this manuscript. There were two drivers that can be traced to two important early career choices. These two drivers also ended up forming the two primary research themes on the functions of the frontal lobes. After a brief review of the reasons for the roads chosen in my career path, a summary of the two themes of research is presented.

Choosing a Career Path

How does one choose a career? The career one of your parents had? A career that will make you the most money? Or did you always know you would be a doctor or lawyer or psychologist, in almost a predetermined way?

Suppose you somehow did choose psychology as your general route. Every student then faces the dilemma of what specific research area to study, or which clinical disorder on which to focus: supervisor's topic (some supervisors give no choice—so the decision of a supervisor must come early); hottest current topic; the topic most likely to make you famous, or rich; or the thesis question easiest to complete?

There is also the “fire in the belly” approach, the one that responds to burning questions that drive you. Life can create these “drivers” in various ways. In my case, there were two early life decisions that became the motivators (the rationale behind these early life decisions is a totally different topic!). Each career choice reflects a type of focus, and inculcates different modes of thinking and acting. I first started as a monk, intent on a career of quiet, reflection, logic, self-awareness, and big picture thoughts, with academic skills honed in philosophy and theology. My second career was as a high school teacher, teaching physical education, English grammar and literature, and Latin. This eventually morphed into an involvement in student counseling. This career taught both precision in thinking (English grammar and Latin), and action (Physical Education).

These career choices can be ends onto themselves. The transformation came in response to external factors. The high school counseling led to courses in clinical psychology, since many teenagers had problems far beyond requesting advice as to their career choices. It was during that period that the external trigger occurred. There was a push for a scientific base for reforming the education system, and teaching teachers how to teach. The hot neuroscience theory of that period was left brain/right brain. Teachers were told that they should not be too formulaic, and should allow students to be creative and spontaneous. The creative right brain needed opportunities to flourish and develop. Classrooms became open; classes became less structured.

This was not the way I taught, and by most accounts, even reports from my most difficult students, I was a good teacher. However, I could not counter the science argument based on just my personal experience. I needed a rationale that would support the success of my teaching style. The memory of the temporal unfolding of events is a bit vague, but the content is not. By some fortunate event, I stumbled upon Vygotsky, who had a theory of education that seemed to provide a rationale to what I was doing spontaneously. External structure, which was taught to be internalized, was key to the development of independent thought—and for instilling creativity.

But how would such a theory stand against the strength of knowledge of how the brain worked? Reading Vygotsky eventually led to Luria. Reading Luria suggested the importance of the frontal lobes. So, this philosopher, English and Latin teacher, who struggled with mathematics and sciences in high school, who had virtually no University science courses (and these two were by far my lowest marks), started to read papers on the neuroanatomy and connectivity of the frontal lobes: Nauta, Pandya, Barbas, Yeterian, and so on. The anatomy literature strongly suggested that all behavioral/anatomical roads—for example perceptual, linguistic, conceptual, emotional—led to the frontal lobes in a reciprocal manner that in totality could not be matched by any other brain region. Clearly, the frontal lobes have to be central to brain organization, maximizing of brain abilities, and for brain development—all central themes of education.

But what do the frontal lobes actually do? This was still the era of the “riddle of the frontal lobes,” the “paradox of the frontal lobes,” although significant progress was being made. The frontal lobes clearly were important—Sedes Sapientiae, the seat of wisdom—was one term used to describe the role of the frontal lobe. The unpacking of the mystery had not been completed.

The choice of career then was made—the understanding of the frontal lobes, to explain how maximizing brain abilities through development should occur. One unfortunate side-story—it is highly unlikely that the path I was able to follow, could be carved out today.

How to proceed? I continued with my clinical psychology degree (I intended to return to teach high school, now equipped with adequate tools for counseling students). I completed all my clinical psychology courses, then switched to medical courses. Along the way, I slowly started to develop skills and knowledge in neurophysiology (sleep research, event-related potentials), neuroanatomy (went to the medical faculty and convinced the administration to allow me to take pharmacology, neuroanatomy and advanced neuroanatomy—with no science or medical background), and also neuropsychology (Halstead–Reitan). After completing my Ph.D. in the electrophysiology of human concept learning (i.e., event-related potentials associated with learning and performing the Wisconsin Card Sorting test, an early attempt to understand frontal lobe functioning using an imaging modality; Stuss & Picton, 1978), I decided to continue my education with a postdoctoral fellowship. One other observation relevant to a career path and the winning of the NAN prestigious award—all of my degrees are from one university, the worst decision that one could make in planning a fruitful career that would eventually result in a lifetime achievement award. The inference is this—the ideas were the drivers, not an idealized career path.

I was advised to apply to the Boston VA Hospital for a postdoctoral fellowship. Coming with my own funds from Canada might make a difference. I remember my interview with Harold Goodglass quite clearly.

What type of research do you do, he asked? Evoked potentials. Too bad, he replied, we do not have any evoked potential research here. What else? Electrophysiological manifestations of sleep disorders. Too bad. What neuropsychological training have you had? Halstead-Reitan. Too bad (I think with an eyebrow lifted!). What type of neuropsychological phenomena interests you? Frontal lobe functions. Too bad—we are an aphasia research center, and also do memory research. There are no frontal lobe patients here at the Boston VA.

Too bad, indeed. At least four “too bads.” As I stood up to leave, dejected, Dr. Goodglass (as I called him for a long time) said: Can you start in September—we will have space then. He and I talked for years after about the reasoning behind his decision—he was never quite sure himself.

The following are my frontal lobe publications arising directly from my time at the Boston VA, a training center that “had no frontal lobe patients” (Alexander, Stuss & Benson, 1979; Benson & Stuss, 1982; Benson et al., 1981; Naeser, Levine, Benson, Stuss & Weir, 1981: Stuss & Benson, 1983, 1984, 1986; Stuss, Alexander, Lieberman, & Levine, 1978; Stuss, Benson, Kaplan, Weir, & Della Malva, 1981; Stuss, Kaplan, et al., 1981; Stuss et al., 1982, 1983, 1986; Stuss, Benson, Kaplan, Della Malva, & Weir, 1984). I even was fortunate to do some aphasia research (Goodglass & Stuss, 1979, 1980), and research on event-related potentials (Stuss, Toga, Hutchison & Picton, 1980), including of naming in aphasic patients (Stuss, Goodglas, Knott, & Sax, 1978). John Knott, a pioneer in the field of evoked potentials, happened to be quietly working in the Boston VA Hospital, and no one seemed to be aware of his presence or background. Dr. Goodglass hired an outstanding student from MIT to be my engineering guru, and paid for a research assistant.

Many lessons were learned from the doctoral and postdoctoral training experience, although which ones were most important were sometimes uncertain. Success appears to favor a prepared mind; driven curiosity opens eyes to opportunities; success requires champions; luck is essential. What is certain—teams with complementary strengths often achieve much more than the sum of the individual contributors, and any success achieved is as much due to colleagues over the years as individual effort.

One Journey, Two Different Routes

The journey was directed to understanding the frontal lobes; the personal drivers bifurcated the path into two routes—the teaching and the reflective routes. Since the revelation of the importance of the frontal lobes initially came though the study of the anatomical organization and connectivity of this region with other brain regions, the experimental methods always stressed the anatomical relation to function. There are different methods one can use to study the frontal lobes. My preferred method was lesion research. The curiosity as to which frontal region was necessary for a specific process or even task (which can only be answered by having the region inactive, only possible at that time by damage to a region) was more central to my quest than the question of which regions are activated.

The Teaching Route

How you use the knowledge of brain functioning as a guide to education principles will depend on what question you ask. As a teacher, I was less interested in content and more in teaching how to think: how to analyze a problem, understand and focus on the core issue, organize and write a response, and “staying on task” over time. The courses I taught, particularly English grammar and Latin, were perfect for inculcating these strategic abilities, as Vygotsky himself noted. In current neuroscience parlance, the domain general processes were more important than the domain-specific processes—hence the interest in the frontal lobes.

In the beginning stages of my research career, a major question was this: if the frontal lobes have a dominant central organizing role, is this system unitary (an “executive”) or fragmented (a series of domain general control processes)? In 1995, Stuss, Shallice, Alexander and Picton, the right team (from my perspective), summarized the existing frontal lobe lesion literature. We analyzed the tasks used in previous lesion research, and suggested that they could be grouped into categories of tasks with specific operational definitions. We went one step further—we concluded that each of the tasks such as sustained attention was not representative of a process but rather were descriptions of complex tasks requiring multiple processes. Using Norman and Shallice's (1986) Supervisory System as the framework, we then hypothesized that performance on any of the tasks could be broken down into a combination of five separate component supervisory (frontal lobe) processes that would interact with lower level schemata. We labeled these energization of the target schema, inhibition of irrelevant schemata, adjustment of contention scheduling which are the lateral inhibitory mechanisms controlling competition between schemata, monitoring of schemata activity, and control of “if–then” logical processes.

Our mission then was to find evidence for these five processes. In designing new tasks we went against the common wisdom. The teaching had always been that the frontal lobes were necessary primarily for complex tasks, or in new situations. Complex tasks, however, are by their very nature multi-factorial in process demands, and our goal was to isolate individual processes. We bucked the trend by creating tasks that were at their core very simple, and then scaffolded difficulty onto a simple core. We expected the simplest level of task to be too easy to require the functions of the frontal lobes, but this lowest level would serve as a control measure for the more complex demands added onto the core. When reading the papers, it will be very clear that we were very fortunate in taking this gamble—the approach was correct even if our specific hypothesis was somewhat lacking—frontal lobe processes are evident even in very simple tasks.

The tests themselves and results are described in a series of articles (Alexander, 2006; Alexander, Stuss & Fansabedian, 2003; Alexander, Stuss, Shallice, Picton & Gillingham, 2005; Alexander, Stuss, Picton, Shallice & Gillingham, 2007; Eskes, Szostak & Stuss, 2003; Floden & Stuss, 2006; Floden, Alexander, Kubu, Katz & Stuss, 2008; Floden, Vallesi & Stuss, 2011; Picton, Stuss, Shallice, Alexander & Gillingham, 2006; Picton et al., 2007; Shallice, Stuss, Alexander, Picton & Derkzen, 2008a; Shallice, Stuss, Picton, Alexander & Gillingham, 2008b; Shallice, Stuss, Picton, Alexander & Gillingham, 2008c; Stuss, 2006, 2011; Stuss & Alexander, 2007; Stuss et al., 1994,1998, 2000; Stuss, Floden, Alexander, Levine, & Katz, 2001a; Stuss, Binns, Murphy & Alexander, 2002a, 2002b; Stuss, Murphy, Binns, & Alexander, 2003, 2005; Wheeler & Stuss, 2003). We found reliable evidence, replicated between different types of tasks both experimental and clinical, across different groups of patients, and across different modalities, for three separate attentional processes within the frontal lobes: superior medial—Energization; left lateral frontal—task setting (criterion setting, planning); right lateral frontal—monitoring (see Fig for a summary). We consider only the last two to represent the common definition of executive function (e.g., Lezak, 1995, p. 42, 1006)

Energization

Energization is defined as the process of initiation and sustaining any response, thereby facilitating the neural systems needed to make decisions and initiate responses. Patients with superior medial (primarily in areas 24, 9 and 6) damage were significantly slower than all other frontal damaged patients on speeded tasks. This was reflected in different measures, including slowness in responding to a simple external stimulus, a disproportionate decline in words during the last 45 s of a letter fluency task compared with the first 15 s, and impairment in sustaining the beneficial effects of a warning signal over a 3-s period (Alexander et al., 2005; Stuss et al., 1998, 2005, 2002a).

Executive Functions

Two processes do fit a definition of executive functions.

Monitoring

Patients with right lateral damage, primarily in areas 44, 45, 46, 9, 9/46, and 47/12, had impaired monitoring, defined as the process of checking a task over time for performance quality as a prerequisite for adjustment of behavior. Impairment was exhibited as increased individual variability of performance especially over time, impaired foreperiod effect, and an increase of all types of errors, including false negatives. This combination suggested poor monitoring of ongoing performance on very different tasks (Picton et al., 2006; Stuss et al., 2005, 2002a).

Task Setting

Task setting is the ability to set a stimulus–response relationship, which would include formation of a criterion to respond to a defined target with specific attributes, organize the programs (schemata) to complete a specific task, and adjust contention scheduling such that the automatic processes of completing the steps of a task work smoothly. Patients with comparable left lateral damage had impaired task setting, exhibited by increased false positives (poor criterion setting) in any task (e.g., Stroop, word list learning, etc.). As expected, most of the difficulties were most prominent in the initial stages of learning (WCST, ROBBIA concentrate, and ROBBIA suppress) (Alexander et al., 2005; Shallice et al., 2008b,c).

There are important observations and corollaries associated with this program of research. First, these dissociations make perfect anatomical sense based on frontal–subcortical connectivity (Alexander, Delong & Strick, 1986). There are five frontal–subcortical circuits. Two are associated with motor functions. Two of the other three proposed by Alexander and colleagues map directly (functionally and anatomically) onto energization and executive functions (the third is presented below). This is similar to the proposal by Cummings and colleagues (Cummings, 1993; Mega & Cummings, 2001), with the exception that they use the term “executive” for all three of the nonmotor frontal processes, and we restrict the use of that term just to those functions (task-setting/planning, monitoring) most applicable to the psychological definition of executive.

Secondly, once the brain-behavior associations were established, we could pursue how these regions perform in neurologically normal individuals. The relation of the same processes to the same regions have now been replicated using functional magnetic resonance imaging (fMRI; Vallesi, McIntosh, Alexander, & Stuss, 2009; Vallesi, McIntosh, Crescentini, & Stuss, 2012; Vallesi, McIntosh, Shallice, & Stuss, 2009), adding another level of validation for the dissociations. Thirdly, the discovery of deficits in specific processes related to defined brain region on tasks that seemed “nonfrontal” in their demands was somewhat surprising. Clearly, frontal lobe processes are domain general supervisory processes important for all types of tasks, even apparently simple tasks, particularly in the initial stages of engagement in the task.

Finally, how do these finding apply to education? These results imply that it is important to understand the total complexity of brain functioning as related to how one trains brain abilities. Our research program stressed the importance of the role of the frontal lobes in directed integrated brain functioning, possible because of its anatomical interconnectivity. There are separate frontal lobe attentional processes, not just a general control. And as Luria (1973) suggested with his construct of verbal regulation of behavior (e.g., task setting!), these can be taught.

The Reflective Route

The same groups of patients, for the same basic anatomical reasons, allowed the pursuit of brain processes important for self-reflection of whom we are, and our roles in life.

Let' us return to anatomy. In the teaching route, the dissociation of processes was reinforced by anatomical connectivity. Evolutionary development of the brain provides additional information on why and how the frontal lobes are fractionated (Pandya & Barnes, 1987; Pandya & Yeterian, 1996; Sanides, 1971; Stuss & Levine, 2002). As the brain develops, there are two broad anatomical paths, and each of these can be related to a distinct category of frontal lobe functions. One developmental path stems from the hippocampus which evolved into the lateral frontal executive processes. There is therefore an anatomical reason why the lateral frontal regions are related to executive functions within the frontal lobes.

Emotional and Behavioral Self-Regulation

The second developmental trend derives from the olfactory region, and this evolved into orbitofrontal/ventral medial regions. This latter region is involved in emotional and behavioral regulation. Thus, just based on how the brain has developed, there are two main divisions of function within the frontal lobes: executive—lateral frontal cortices; behavioral/emotional—orbitofrontal/ventral medial regions.

Damasio and colleagues (Bechara, Damasio, Tranel, & Damasio, 1997; Bechara, Damasio, Damasio, & Lee, 1999; Oya et al., 2005; Koenigs et al., 2007; Young et al., 2010) have been pioneers in understanding the social/emotional roles of the regions of the frontal lobes related to developing appropriate emotional reactions and social behaviors. Patients with damage to the ventromedial cortex (VMPFC—areas 32, 25, 24, 14, 13, 12, 11) often have normal performance on commonly used tests of executive functioning but significant difficulty with integrating the motivational, reward/risk, emotional, and social aspects of behaviors (e.g., Stuss & Benson, 1983) more than with the executive functions required to implement a behavior—deception, empathy and gambling tasks (Bechara, Damasio, Damasio & Anderson, 1994; Bechara et al., 1999; Stuss, Gallup & Alexander, 2001b). All involve reward/risk processing of sorts, for the individual or for others (see also Rolls, 2002). However, the tasks are complex and await identification of the fundamental processes (e.g., Floden et al., 2008), some perhaps “executive” (Manes et al., 2002).

Metacognitive/integrative processes

It is area 10 that was most mysterious, one of the very last regions to evolve. D. Pandya in the early 1990s had suggested in discussions that this was an integrative region above and beyond the integrative role of the rest of the frontal lobes. Area 10 does not have extensive anatomical connectivity with the posterior regions of the brain; rather, the connectivity comes primarily with the dorsal and ventral streams of frontal lobe functioning. In the reflective route, then, we looked for ways of assessing and identifying specific frontal behavior associations in a manner similar to the way we did in the teaching route. In collaboration with Gordon Gallup (another example of the importance of having collaborators) in the early 1990s, we investigated the potential role of the frontal lobes in functions such as behaving from the perspective of another to make inferences about the world and recognizing the differences between what one knows from what one infers, believes, or remembers (e.g., theory of mind) (Rosenbaum, Stuss, Levine & Tulving, 2007; Stuss et al., 2001b) and understanding humor (Shammi & Stuss, 1999).

The primary function of area 10 appears to be integrative and coordinating—orchestrating the energization, motivation, emotional perspective, and executive capacities that are necessary to accomplish complex, novel tasks. Damage to polar regions (10s and 10i) impairs these integrative functions (Burgess, Gilbert & Dumontheil, 2007), although how to dissemble this putative function from the effects of VMPFC lesions is sometimes not certain.

Summary

Following the personal influences that evolved into two parallel research interests led to findings that were important in concluding that the frontal lobes cannot be equated with executive functions. Executive functions are associated only with a specific region of the frontal lobes and other functional categories are associated with other frontal regions. Frank Benson and I had postulated in the 1980s (Stuss & Benson, 1984, 1986) the importance of dissociating brain/behavior relations within the frontal lobes, a concept having considerable similarity to our current position. After many years of research, there is considerable evidence to postulate at least four separate categories of frontal lobe functions, only one of which can be labeled executive: energization (initiation and sustaining of behavior); executive (e.g., task setting, monitoring); behavior/emotional self-regulation; and metacognition (theory of mind/integration) (Stuss, 2011; see also Stuss, Picton & Alexander, 2001). The behavioral evidence for these four categories is supported by the fact that the categories map onto general anatomical localization based on principles of frontal lobe development and connectivity. Somewhat different proposals for a fractionated frontal system also exist (e.g., Godefroy, Cabaret, Petit-Chenal, Pruvo & Rousseaux, 1999; Koechlin, Basso, Pietrini, Panzer & Grafman, 1999; Shallice, 1982; Shallice & Burgess, 1996).

Further refinement of this framework is not only possible but likely (e.g., see D'Esposito & Badre, 2012 for ideas of hierarchy of functioning that could map on the general idea of task-setting). Moreover, fractionation should not imply a pure localizationist approach (Stuss, 2006). These findings also provide a framework for the development of rehabilitation (Levine, Turner & Stuss, 2008).

So, after many years, we concluded that the frontal lobes do not equal a central executive (Stuss, 2011; Stuss & Alexander, 2007). But the frontal lobes do play an important integrative role (like a high school teacher!), possibly because of the extensive reciprocal connections with virtually all other brain regions, integrating information from these regions. And as I had to learn from my experience as a high school counselor, one has to integrate emotional and motivational processes to achieve personal success.

For me, science did mirror reality.

Funding

This work was supported by a Canadian Institutes of Health Research Group Grant to the Rotman Research Institute (# MGC 14974), and Operating Grant (# MT 12853).

Conflict of Interest

None declared.

Acknowledgments

The credit for this manuscript, and as well the NAN award, must be shared with my mentors, colleagues, research assistants, and all those who influenced me over the many years. It should be obvious in the routes followed how my relationships over the years influenced me, with two of these relationships (with T. Picton and M.P. Alexander) continuing for virtually all of my academic life). Indulgence of the reader is requested—since this is not a review of the literature, but a reflection on my own path, the references are primarily those that derive from personal research. Much more detailed information can be gathered from many other sources, including from the two editions of Principles of Frontal Lobe Function, D.T. Stuss & R.T. Knight (Eds.), 2002, 2012.

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