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Exorcising the Homunculus
There’s no one behind the curtain

by David C. Noelle


The following article is from Free Inquiry magazine, Volume 21, Number 2.


Among the issues probed by philosophers, perhaps none strikes closer to home than inquiries into the origins of human action. How do our thoughtful decisions arise, and how are they translated into overt words and deeds? Many of our actions appear to be produced automatically, without deliberation. We need not focus on the precise control of every muscle as we execute a practiced golf swing, and we rarely find ourselves weighing each individual word choice when we utter a request for a condiment during dinner. In the midst of such automatic behaviors, decisions seem to be made for us, enacted by reflexes and learned habits. There are some actions, however, for which we claim authorship. We carefully weigh the options before selecting a particular golf club from our bag, or we purposely edit an amusing tale that might offend those with whom we dine. These controlled behaviors feel more effortful to produce, and we sense that they stem from our conscious thoughts.

The mental faculty responsible for the selection of our controlled actions has traditionally been dubbed “the will.” From the cogitava of Aquinas to the noumenally free will of Kant, philosophers have posited this central faculty as the helm of the body and the mind. The will is said to be where desires and goals are translated into action and where ingrained habits are suppressed in favor of reasoned plans. It has been heralded as the seat of moral thought.

By some accounts, the mind is modular, with the will fairly isolated from other mental faculties. The sources of emotion, world knowledge, memory, learning, and imagination are at the will’s disposal, but are not part of it. Indeed it is thought the will can function, if perhaps clumsily, without these other faculties. The will is also often seen as essentially atomic—a fundamental aspect of the self that cannot be decomposed into other psychological processes.

Unfortunately, asserting that such a will is the source of our actions does little to advance our understanding; it merely introduces a regress concerning the locus of decision making. We started with the question of how the individual makes a choice, and we are left with the question of how the will makes a choice. The will takes on the character of a homunculus—a little man who resides in the mind and acts as the “central executive” of the cognitive enterprise. The homunculus seems to be the ruler of the mind, the maker of choices, and the kernel of identity, but it is truly a useless hypothetical construct that explains nothing about the origin of our actions. If we are to understand our own controlled behavior, the homuncular will must be exorcised from the mind.

That exorcism is currently under way, using the tools of modern experimental psychology and cognitive neuroscience, but it is not yet complete. While a detailed and substantiated account of the mechanisms of controlled behavior is still forthcoming, mounting evidence suggests that what has been traditionally called “the will” is neither largely independent of other mental systems nor functionally localized and atomic in the brain. Instead, current speculations see “executive control”—the array of processes that, for many cognitive scientists, replaces traditional notions of “the will”—as emerging from the concerted interaction of disparate neural circuits.

 

Willful Neurons

While it is easy to introspect and speculate about the varied sources of our thoughts, actually reverse engineering the brain to determine its primary working parts is an incredibly difficult task. The brain has about a hundred billion neurons, each connected to about a thousand other cells; simply producing any sort of a wiring diagram is a monumental project. Even more difficult is finding ways to watch the brain in action. Still, scientists have produced a number of techniques, both behavioral and neuroscientific, for collecting clues concerning the architecture of the mind, and these have been used to discern the structure of executive control.

Experiments have shown that controlled behaviors tend to be slower than their more automatic counterparts, especially when one is trying to inhibit an automatic response. The classic example of this is the Stroop task, in which you are asked to name the color of the ink of a printed word.1  You will tend to be slower to name the ink color if the the printed word is the name of a color (e.g., “green”). The idea is that executive control processes have difficulty overcoming your predisposition simply to read the word that appears before your eyes.

Control is dynamic, allowing you to switch from one behavior to another rapidly and flexibly. But this comes at a cost. You will tend to be slow at a newly engaged task until you “get into the groove” by performing it a bit. Also, the dynamic nature of executive control makes control easy to lose: distractions can cause us to slip into automatic patterns of behavior. Control processes seem to require active maintenance of behavior-guiding information.2  Such a “working memory” system appears to be central to executive control, providing the means to keep in mind what needs to be done. Working memory is also critical to the reasoning and planning processes required to consciously select actions—maintaining intermediate conclusions and goals while the mental gears grind.

In the brain, the frontal lobes appear to be critical for executive control. In addition to housing higher motor areas, the frontal cortex appears to play a central role in working memory, maintenance of goals, selective attention, and strategy generation. Patients with frontal lobe damage exhibit a wide range of behavioral deficits. They have difficulty with fine movements and complex chains of motions. They show problems in flexible problem-solving, attention, and memory. Frontal lesions can produce a tendency to persist with a pattern of behavior after it has ceased to be appropriate, a lack of appreciation for the risks involved in certain actions, and impaired learning. Frontal patients have difficulty inhibiting automatic responses (e.g., they show excessive Stroop interference), they have trouble maintaining mental focus over a delay, and they spontaneously produce fewer actions, in general. In short, the frontal cortex seems to be important for selecting actions appropriately, producing flexible action sequences, keeping relevant information in mind, and overcoming habitual behaviors.3

There is evidence to suggest that frontal systems develop slowly as we mature and deteriorate with old age. Behavioral experiments certainly support this lifetime pattern of performance on executive control tasks. Children and seniors show increased difficulty inhibiting automatic responses and flexibly switching between tasks.4

 

Interdependent Mechanisms

One might be tempted to see the frontal cortex as the home of the traditional will, but reality seems to be less simple than that. It is far from clear that frontal systems are capable of executive control on their own. In addition, the frontal cortex appears to be essential for certain psychological processes unrelated to executive control.

The frontal cortex appears to be important for reasoning and problem solving, but other areas seem critical for these higher functions, as well. Knowledge about the world, mediated in part by circuits in the temporal lobes, is important for problem solving. Visual and spatial reasoning rely on systems in the occipital and parietal lobes of the brain. Still, the frontal cortex seems to play a central role in such activities. Evidence for this includes the observation that prefrontal activity is consistently prompted by a wide range of standardized I.Q. test tasks.5

Traditional conceptions of the will assume that reason and the will are tightly bonded, but posit a greater isolation between the will and the emotional faculties. Emotion, after all, seems to drive many of the kinds of automatic responses that executive control must overcome. There is now reason to believe, however, that emotional systems are critical for effective, reasoned decision-making. This evidence primarily stems from patients with ventromedial frontal lobe damage. These patients score well on standard I.Q. tests, but show marked deficits in practical reasoning skills. They can become stuck on even simple problems, endlessly exploring the options without ever coming to a conclusion. They behave as if they are insensitive to risks, even though they can intelligently discuss such risks. Their reasoning seems to be decoupled from their actions. Importantly, these patients also show a pronounced absence of physiological responses to emotional situations (e.g., sweating or increased heart rate). These cases have caused some neuroscientists to suggest that healthy emotional responding plays a critical role in guiding reasoning processes and in connecting deliberation to action.6 Emotional systems allow conclusions to be reached in a timely manner, and they give conviction to our thoughts. Thus, counter to traditional accounts, emotion appears to be critical for executive control. The armchair philosopher might argue that, since we can conceive of a rational decision-maker free of emotion, the will must be conceptually independent of emotional systems. The brain does not seem to be convinced by this argument, however.

Psychological processes not primarily identified with executive control also seem critically dependent on the frontal cortex. For example, various kinds of learning and memory seem to require frontal support. While memory for recent autobiographical events is often associated with the medial temporal lobe, both brain imaging studies and work with patients have suggested that the frontal cortex actively contributes to storage and retrieval of such memories.7  Frontal working memory systems also appear to be important for explicit forms of learning, such as learning from direct instruction.8

 

Components of Will

In order to banish the homunculus, we must find a way to reduce executive control functions to a collection of more simple psychological mechanisms. While efforts to decompose the circuits of controlled behavior are just beginning, some early findings and speculations are both fascinating and promising.

Some regions of the frontal cortex contain an abundance of cells that are richly interconnected. Computer modeling has shown that such a configuration of connectivity often results in the active maintenance of patterns of neural firing over time.9  In other words, these recurrent connections may form the basis of a working memory system. Neural recordings in nonhuman primates have found such sustained activity in frontal cells, with the activity coding for the properties of recent events that are important for guiding behavior.10  For example, a monkey might be trained to note where a small dot flashes on a screen, only shifting its gaze to that location after a bell sounds. While waiting for the bell, some of these frontal cells actively encode the location of the previously presented dot, holding the location in mind until it is time to act.

Neurons in the frontal cortex send connections to areas throughout the brain. Thus, the “control signals” held in a frontal working memory system are in a good position to modulate processing in a fairly global way: focusing attention in perceptual systems, priming responses in motor systems, and inhibiting inappropriate automatic processes. Some mechanism is needed, however, to determine the kind of control information that should be actively maintained. While there is some evidence to suggest that certain areas of the frontal cortex play a role in the adjustment and manipulation of working memory contents, another candidate for this role lies deep in the brain.

Hiding far beneath the folds of the cerebral cortex, the basal ganglia receive extensive projections from the frontal cortex and, through the thalamus, send extensive connections back. Certain cells in this limbic area can learn to identify events and actions that are predictive of reward.11  For example, if food consistently follows a ringing bell, these neurons will initially fire when food is presented, but will, over time, stop firing for the food and start firing for the bell. Computer scientists have produced model neural circuits that are capable of learning to predict reward in this way and, critically, these models can use such predictions to learn to select appropriate actions for complex tasks.12 (A world-class backgammon playing program sold by IBM learned its strategy using a neural network model of this kind.13)  Through its connections with the frontal cortex, the basal ganglia may also learn to identify the properties of working memory contents that are predictive of reward and may, thus, signal frontal systems to actively maintain exactly those control signals that are needed for success.18

It is interesting to note that the basal ganglia are also thought to be involved in the basic initiation of actions and in the coordination of action sequences. Parkinson’s disease selectively affects this limbic structure, and patients stricken with this ailment have trouble starting motions and switching between well-learned motor sequences. Thus, it is likely that the basal ganglia are involved in both automatic and controlled aspects of the motor system.

Another brain area of importance for executive control is the anterior cingulate cortex. Nestled in the deep fold that separates the brain’s hemispheres, the cingulate appears most active in situations in which there is substantial conflict between competing options—situations where the brain is having a hard time settling on one action or another. Scalp electric field measurements have detected a signal from roughly this area that appears when a behavioral error is made. This error-related negativity appears even when subjects are not told they have made an error but, instead, realize it themselves.19  It is not clear if this cingulate activity is the result of reward prediction information sent there from the basal ganglia or if it is an independent measure of task difficulty.20  In either case, such performance-monitoring information would be useful for selecting both actions and working-memory contents. Some theories see the anterior cingulate as the locus of action-selection processes, modulated by frontal systems. Other theories see the frontal cortex as more central. In either case, the anterior cingulate cortex and the frontal areas work together to suppress automatic responses in favor of explicitly selected actions.

What emerges is a general story in which the frontal cortex sends actively maintained control signals to much of the rest of the brain. The nature of these signals is selected primarily by circuits in the limbic system, based on predictions of reward. The control signals maintained in working memory, along with conflict-related processing in the anterior cingulate, give rise to the selection of appropriate actions for the current situation.

Cognitive neuroscientists have begun breaking down executive control into its functional parts. Much of this research is still speculative, and detailed accounts of such processes as strategy generation and complex action planning have yet to receive much attention. There is still much work to be done.

 

The Power of the Brain Compels You

The traditional view of the will as a kind of little man in your head needs to be replaced by a detailed account of how neural tissue gives rise to controlled behavior. Preliminary attempts to understand the mechanisms of executive control have found that they do not form an isolated psychological faculty, but are heavily dependent on other psychological processes, including emotional response. Initial attempts to dissect the mental executive have identified critical roles for a frontal working memory system and a limbic reward-prediction system. The scientific exorcism of the homunculus continues, hoping to produce a clear view of how mere flesh can give rise to our most deliberate and considered actions.


Notes

1. J. Ridley Stroop, "Studies of Interference in Serial Verbal Reactions," Journal of Experimental Psychology 28(1935): 643-62.

2. Jonathan D. Cohen, Todd S. Braver, and Randall C. O'Reilly, "A Computational Approach to Prefrontal Cortex, Cognitive Control, and Schizophrenia: Recent Developments and Current Challenges," Philosophical Transactions of the Royal Society of London B 351 (1996): 1515-27.

3. Angela C. Roberts, Trevor W. Robbins, and Larry Weiskrantz, eds., The Prefrontal Cortex: Executive and Cognitive Functions (Oxford: Oxford University Press, 1998); and Mark Wheeler, Donald T. Stuss, and Endel Tulving, "Frontal Lobes and Memory Impairment," Journal of the International Neuropsychological Society 1(1995): 525-36.

4. Norman A. Krasnegor, G. Reid Lyon, and Patricia S. Goldman-Rakic, eds., Development of the Prefrontal Cortex: Evolution, Neurobiology, and Behavior (Baltimore: Brookes Publishing, 1997).

5. John Duncan, Rudiger J. Seitz, Jonathan Kolodny, Daniel Bor, Hans Herzog, Ayesha Ahmed, Fiona N. Newell, and Hazel Emslie, "A Neural Basis for General Intelligence," Science 289, 5478 (2000): 457-60.

6. Antonio R. Damasio, Descartes' Error: Emotion, Reason, and the Human Brain (New York: G. P. Putnam, 1994).

7. Lars Nyberg, Endel Tulving, Reza Habib, Lars-Goran Nilsson, Shitij Kapur, Sylvain Houle, Roberto E.L. Cabeza, and Anthony Randal McIntosh, "Functional Brain Maps of Retrieval Mode and Recovery of Episodic Information," NeuroReport 7(1995): 249-52.

8. David C. Noelle, "A Connectionist Model of Instructed Learning," Ph.D. thesis, University of California at San Diego, Department of Computer Science and Engineering, Department of Cognitive Science, 1997.

9. Daniel J. Amit, Modeling Brain Function: The World of Attractor Neural Networks (Cambridge, U.K.: Cambridge University Press, 1989).

10. Earl K. Miller and Jonathan D. Cohen, "An Integrative Theory of Prefrontal Cortex Function," Annual Review of Neuroscience, in press.

11. Wolfram Schultz, Paul Apicella, and Tomas Ljungberg, "Responses of Monkey Dopamine Neurons to Reward and Conditioned Stimuli During Successive Steps of Learning a Delayed Response Task," Journal of Neuroscience 13(1993): 900-13.

12. P. Read Montague, Peter Dayan, and Terrence J. Sejnowski, "A Framework for Mesencephalic Dopamine Systems based on Predictive Hebbian Learning," Journal of Neuroscience 16(1996): 1936-47.

13. Gerald Tesauro, "Temporal Difference Learning and TD-Gammon," Communications of the ACM 38(3) (1995).

18. Todd S. Braver and Jonathan D. Cohen, "On the Control of Control: The Role of Dopamine in Regulating Prefrontal Function and Working Memory," in S. Monsell and J. Driver, eds., Attention and Performance XVII (Cambridge, Mass.: MIT Press, 2000).

19. William J. Gehring, B. Goss, Michael G. H. Coles, David E. Meyer, and Emanuel Donchin, "A Neural System for Error Detection and Compensation," Psychological Science 4(1993): 385-90.

20. Matthew Botvinick, Leigh Nystrom, Kate Fissell, Cameron S. Carter, and Jonathan D. Cohen, "Conflict Monitoring Versus Selection-for-Action in Anterior Cingulate Cortex," Nature 402(1999): 179-81; and Clay Holroyd, Jesse Reichler, and Michael G.H. Coles, "Is the Error-Related Negativity Generated by a Dopaminergic Error Signal for Reinforcement Learning? Hypothesis and Model," in Cognitive Neuroscience Society Annual Meeting Program, p. 45, Washington, D.C., 1999.


David Noelle is a postdoctoral research associate at the Center for the Neural Basis of Cognition, a joint project of Carnegie Mellon University and the University of Pittsburgh.


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