Objectivity? A Role For Emotion In Decision Making

One of the reasons I like listening to Public Radio is that they provide a lot of clinicopathological case material that is usually quite illustrative, and frees me from the huge hurdle of being suspected of disclosing confidential patient information on this blog.  Just a note on the historical context.  When I started out, deidentified clinical information was a mainstay of teaching.  It was presented at case conferences and in medical journals.  At some point that became a lot less likely and in my opinion that adversely affects teaching in a way that could be dangerous to the health of patient.  The best physicians depend on pattern matching to recognize diseases and many of those patterns are recalled not just from live patients but also pictures, images, and numbers that are remembered independent of any real contact with a live patient.  When an administrator did not allow me to use deidentified MRI scan images for teaching residents, those residents end up knowing a little bit less, not in terms of book learning but in terms of the experiential aspects of medicine.  The most unique technical skill that your physician has that nobody else does is access to a vast array of patterns that were experienced in medical school and post graduate training.

I was driving around today, listening to public radio when a show came on called Radiolab.  I have heard it before and it is interesting because it tried to present science in interesting ways and in many cases that involves medicine.  Today's show was all about choices and I happened to pick it up about 1/3 of the way in or roughly the 20 minute mark.  At that point Antoine Bechara, MD, PhD began discussing the case of Elliot, a young accountant.  Elliot was working for a corporation as a successful upper level manager.  He was married and had children.  He was considered to be smart, successful, and religious.  One day a small tumor was discovered in his orbitofrontal cortex and it was successfully removed.  Post surgical neuropsychological testing showed that was still in the 97th percentile in terms of IQ testing.  He returned home and then went back to work.

What occurred following the successful neurosurgery was unexpected.  He was no longer able to make even routine decisions.  As an example, when he tried to decide what pen to use to sign a contract, it took him 30 minutes to decide whether to use a black pen or a blue pens.  All possible permutations of the decision were explored and evenly considered.  In the case where many more choices were available (the program used the example of a breakfast cereal aisle in the grocery store), the decisions became more impossible.  He was so disabled by this problem that he lost his job and eventually his marriage and family.   He got involved with a con man.  He lost his savings and went back to live with his parents.  Somewhere along the way he was seen by the behavioral neurologist Antonio Damasio, MD, PhD who tested him with visual stimuli designed to elicit strong emotional responses.  These visual stimuli failed to elicit these responses in the patient.  Damage to his orbitofrontal cortex had caused this disconnection.  Disconnecting the emotional response resulted in an impairment in decision making rather than an expected improvement.  Without the feeling state he was pathologically indecisive.

Major Anatomical Connections of the Ventral Medial Prefrontal Cortex from:  Euston DR, Gruber AJ, McNaughton BL. The role of medial prefrontal cortex in memory and decision making. Neuron. 2012, figure 3 with permission.

When I heard Dr. Bechara talking I remembered an excellent presentation that he gave on how people with addictions tend to respond to the Iowa Gambling Task (GT) and how some responses in that paradigm are consistent with increased risk for substance use.   This test looks at subjects attempts to optimize a $100 bet on choices from 4 decks of cards (A, B, C, and D).  The subject is to make 100 card selections in any order from any of the decks.  A selection from deck A or B results in a $100 reward.   There are unpredictable punishments so that the subject loses $1250 in every 10 cards selected from deck A or B.  Selections from decks C and D result in a $100 reward with unpredictable punishments resulting in a loss of $250 in every 10 cards from decks C and D.  The penalties are not fixed and some of them are substantial.  Take a look at this video for an example of how it works (the initial sum used in the video is substantially higher than quoted in the research literature).  Normal subjects eventually learned that they are more likely to get punished choosing from decks A and B and they will gravitate toward decks C and D.  The Iowa group used this test paradigm and modifications to investigate aspects of decision making in the ventromedial prefrontal (VM) cortex (bilateral lesions to the gyrus rectus, mesial half of the orbital gyrus and the inferior half of the medial prefrontal surface).

Subjects with lesions in the VM do not reduce their selection of decks A or B or increase their selection of choices in decks C and D.  The impairment in decision making can be replicated over time.  In order to investigate whether any emotional process was involved, the investigators looked at skin conductance resistance (SCR) associated with the decisions.  They looked at a window of +/- 5 seconds on either side of the decision to examine anticipatory, reward and punishment SCRs.  Normal subjects develop anticipatory SCR and they are more pronounced before selections from the disadvantageous decks (A and B).  Even the 20% of normal subjects who are self professed risk takers develop anticipatory SCRs but they are lower in magnitude when selecting for the disadvantageous versus advantageous decks.   VM subjects had no anticipatory SCR suggesting that these patients had a compromised ability to change their somatic state (skin conductance) in anticipation of an imagined scenario in an uncertain condition.

The researchers also looked at the question about whether biases in this paradigm were conscious or not.  The experiment in this case used the same decks A, B, C, and D but the task was broken up into 4 different zones.  The subject was asked about their explicit knowledge of what was happening in the game after every 10 cards.  The 4 periods included:

1.  Pre-punishment period before encountering punishment.
2.  Pre-hunch period as punishment was being encountered by the subjects till had no ideas about the game.
3.  Hunch period where guesses about favorable decks begin to appear.
4.  Conceptual period when they have a clear idea about the advantageous versus disadvantageous decks.

In normal subjects the SCRs were absent pre-punishment but began to build and was sustained.  Although 30% of controls never got to the conceptual periods they all had SCRs and played the game correctly.  50% of VM subjects got to the conceptual stage in that they could explicitly state the deck types.  That did not result in them correcting their choices.  In real life this means the patient with frontal lobe damage has an awareness of what is right and what is wrong but the correct choice is not made.  The authors use the example of a person with a substance use disorders balancing the choice between taking a drug as an immediate reward and the long term reward of a stable home, family and work life they choose the drug.  The GT has been used to study the issue of substance users and impairment in decisions is noted.  

The wiring and impact of various signaling systems on the vmPFC is complex.  It is hard to imagine methods that would allow the isolation and correlation of any of these systems suggested in the clinical vignette about the patient with the brain tumor.  The neuroanatomy is also complex.  Many of us were taught to consider the supraorbital area of frontal cortex to be typical frontal cortex,  It turns out that the most medial gyri that represent the vmPFC and are more appropriately considered limbic cortex.   Looking at a recent post on the involvement of the nucleus accumbens in decision making now provides two avenues for advancing decisions - emotions and reward pushing these decisions forward.

Apart from psychiatric disorders and addictions, these brain systems have profound implications for everyday life and the illusion of free will.  Many of the biases in everyday life that many of us would deny that we have, may be the product of the reward and/or emotional valence assigned to that string of associations through these mechanisms.  Many of these biases are unconscious.  I think there is widespread confusion that emotions compromise objectivity (as in rational decision making).  One of the main outcomes of these studies is that emotions are necessary make a decision and do not necessarily compromise the rational aspects of that decision.  The other approach I see written about is the idea that there is a reptilian brain lying deep inside the human brain and this has a characteristic response pattern (anger/rage).  It was popular to talk about reptilian brains when I first learned neuroanatomy, but a lot less was known about the integration of the human brain at that time.



George Dawson, MD, DFAPA


References:

1:  Radiolab:  Choice

2: Bechara A, Damasio H, Damasio AR. Role of the amygdala in decision-making. Ann N Y Acad Sci. 2003 Apr;985:356-69. Review. PubMed PMID: 12724171.  From a special ediction of the journal called: THE AMYGDALA IN BRAIN FUNCTION: Basic and Clinical Approaches

3: Bechara A, Damasio H, Damasio AR. Emotion, decision making and the orbitofrontal cortex. Cereb Cortex. 2000 Mar;10(3):295-307. Review. PubMed PMID: 10731224.  This is from a special edition of this journal called:  The Mysterious Orbitofrontal Cortex

4: Euston DR, Gruber AJ, McNaughton BL. The role of medial prefrontal cortex in memory and decision making.  Neuron. 2012 Dec 20;76(6):1057-70. doi: 10.1016/j.neuron.2012.12.002. Review. PubMed PMID: 23259943; PubMed Central PMCID: PMC3562704.

Supplementary 1:

Figure 3 above was reprinted from Neuron, Vol. 76 edition number 6, Euston DR, Gruber AJ, McNaughton BL. The role of medial prefrontal cortex in memory and decision making, Copyright (2012), with permission from Elsevier.  License # 3542200221086 License date Jan 04, 2015 per the Copyright Clearance Center.

Supplementary 2:

I use the following human neuroanatomy text by Paxinos and Mai with the accompanying Atlas of the Human Brain by Jürgen K. Mai, Joseph Assheuer, and George Paxinos.  It was recommended to me by Lennart Heimer after I took one of his courses in brain dissection at Washington University.  I requested permission from the publisher to use some of these figures for teaching purposes and the fees were astronomical.  So the text and atlas are primarily useful to clarify your own thinking rather than preparing presentations.

A Head Full Of Prior Probabilities

I read an article in Science recently that reminded me of why I am a subscriber.  The article had to do with a model of rational thinking based on the neurobiology of the several critical brain structures, the prefrontal cortex (PFC), dorsal striatum, ventral striatum, and anterior cingulate cortex.  The interesting aspect of this model is that is also takes into account Bayesian analysis and uses that to build a model for how the can make use of these unique neuroanatomical local structures and come up with novel solutions in uncertain environments.

For about 15 years I taught a course that was designed to minimize diagnostic errors when physicians consider the question:  "Is this a medical condition or a psychiatric disorder?"  On of the first cases I would use is a hypothetical case of a teenage girl admitted to a hospital for dehydration secondary to acute gastroenteritis.  In this case the psychiatrist is consulted because the patient began to manifest acute agitation.  This was an acute behavioral change and that was confirmed by family members who had never seen the patient like this before.  The consult to the psychiatrist read: "Please see to assess and treat hysterical behavior."

On the diagnostic side there are several prior probabilities to consider.  In medicine, I like to consider prior probabilities as those of a particular finding or condition that exists is a particular population in the wild.  In this case a few to consider would be:

1.  The prior probability of "hysteria" in teenage girls with no previous behavior problems.  What is hysteria?

2.  The prior probability of acute mental status changes in teenagers with no medical conditions.

3.  The prior probability of teenage girls with no medical problems being in a hospital bed being rehydrated with I.V. fluid therapy.

4.  The prior probability of acute mental status changes in teenagers with no psychiatric or substance use disorders.

Considering 1-> 4, it should be evident that all of the corresponding probabilities are very low.  It would difficult to rank order them on that basis and it suggests the need for more hypothesis generation or data acquisition.   As we examine the patient we realize that cannot produce any meaningful verbal response, she has opisthotonic posturing and decorticate posturing on the left in response to painful stimuli.  The next set of prior probabilities is more declarative:

1.  The posterior probability of a brain problem with opisthotonic posturing and findings 1 - 4.

2.  The posterior probability of an acute brain problem with decorticate posturing and findings 1 - 4.

Suddenly with the examination findings - one specific and the other not - the probabilities of a severe life threatening brain problem have gone through the roof.  The patient appears to be acutely encephalopathic with an impending brain stem herniation syndrome.  This is no longer a patient who should be in a non-acute care bed in the hospital or a patient who needs acute psychiatric care.  She belongs in an intensive care unit, hopefully one that specializes in treating acute, life-threatening neurological disorders so that the problem of increased intracranial pressure can be addressed.  That important decision is made with a two minute examination of the patient at the bedside.  She is transferred to a neurological ICU for more appropriate care.

Without going into too many details about Bayesian inference other than this example, I have never really seen it referred to from a neurobiological perspective.  The new paper by Donoso, et al makes the connection in the introductory paragraphs:

"Human reasoning subserves adaptive behavior and has evolved facing the uncertainty of everyday environments. In such situations, probabilistic inferential processes (i.e., Bayesian inferences) make optimal use of available information for making decisions. Human reasoning involves Bayesian inferences accounting for human responses that often deviate from formal logic (1). Bayesian inferences also operate in the prefrontal cortex (PFC) and guide behavioral choices (2, 3). Everyday environments, however, are changing and open-ended, so that the range of uncertain situations and associated behavioral strategies (i.e., internal maps linking stimuli, actions, and expected outcomes) becomes potentially infinite."


The Wisconsin Card Sorting Test (WCST), a well known neuropsychological measure of frontal lobe mental flexibility.  In the test the subject's task is to sort cards based on shapes, colors, or the number of objects per card.  The sorting paradigm is not made explicit and every time the examiner changes it, the test subject needs to figure it out and start sorting cards according to that new paradigm.  Results can be correct, exploratory, incorrect or perseverative.  Perseverative can be defined as a continuous repetitive sorting error that does not take into account the need for error correction - continuing to use a response that was at one point correct.

At this point there are many imaging studies that look at correlates between functional brain scans and performance on the WCST.  In this study the authors look at a custom variation of the sorting tests where subjects were looking for digit combinations by trial and error and produce a response that was exploratory, perseverative or correct based on feedback about the correctness of choices.  All subject were young (18-26 years old) and screened for medical, neurological, and psychiatric disorders).  There were a total of 40 test subjects equally split by sex.  The article contains a detailed discussion of the subjects response patterns relative to a theoretical model, but I am most interested in the brain imaging results and the implications of those results.

Working in the addiction field, it is fairly common these days to read research studies that look at activation of the ventral striatum.  There are also theories about which neural circuits are responsible for most aspects of addiction including the initial euphorigenic effects,  acute behaviors involving positive reinforcement, and chronic compulsive effects associated with negative reinforcement.  I think that there is an general conceptualization that there are varying levels of euphoria associated with activation of the ventral striatum whether that is from an addictive drug or what has been considered to be "natural" activators of the ventral striatum including food, water, sexual behavior, and social affiliation.  This is the first study that I have seen showing that activation of the ventral striatum is associated with the cognitive aspects of life.  In correspondence with the lead author Etienne Koechlin his group refers to this as the "Eureka Response".  He suggests that the ventral striatum adds and affective valence to a cognitive strategy that has been selected by the frontal cortex as a correct strategy and that  valence contributes to consolidation in long term memory.  He points out that the cognitive system needs the affective role of the ventral striatum to run properly.

If this paper can be replicated this is really landmark work.  It provides a neurobiological explanation for why we can choose among several prior probabilities in important situations.  In terms of clinical decision making it may be why senior clinicians have immediate associations to critical cases when they are involved in subsequent clinical decision making.  That process has been looked at in terms of pattern matching and pattern completion in the past but an affective valence adds another important dimension.

This is potentially one of the most important papers and theories I have seen in recent times.  It has broad implications for psychiatry, addiction, cognitive psychology, and many other fields.  An affective valence from the ventral striatum may make living with a head full of prior probabilities - a lot easier.


George Dawson, MD, DFAPA



Supplementary 1:  The following table lists the common neuroanatomical abbreviations used in this paper:

References:

1: Donoso M, Collins AG, Koechlin E. Human cognition. Foundations of human reasoning in the prefrontal cortex. Science. 2014 Jun 27;344(6191):1481-6. doi: 10.1126/science.1252254. Epub 2014 May 29. PubMed PMID: 24876345.


2:  Albert DA, Munson R, Resnick MD.  Reasoning in Medicine: An Introduction To Clinical Inference.  The Johns Hopkins University Press.  Baltimore. 1988.

"Our aim is to dig deep into the clinical mind and lay bare the processes of reasoning and inference that are (or can be) involved in arriving at and in justifying clinical decisions."

Outlaw Dog Owners And The Psychopathology Of Everyday Life

Before going any further, I have to disclose that I have my own biases about dogs.  In grade school a weimaraner ran up and chomped directly into the side of one of my friends, just below his rib cage.  In another incident an allegedly friendly cocker spaniel leapt up and tore into the throat of another friend as he was bending over to pet him.  Luckily major vessels were missed but it took 80 stitches to close the wound in his neck just below the chin.  I was constantly harassed on my way to school by a dog named Spot.  Spot was a solid black dog, so the name never made any sense to me.  I only had about 6 blocks to walk, but on block 2, Spot would come tearing out of the back yard.   He was menacing, threatening, and attempting to bite.  I didn't think of it at the time, but Spot's owners often just sat on the front porch pretending to be oblivious to their dog's uncontrolled behavior. At times they would utter an unethusiastic: "Here Spot."  But some of my fellow pedestrians took a more aggressive stance with Spot.  I heard that he was kicked and thrashed with a belt.  I was a nervous and wildly neurotic kid so I immediately took a parallel route to avoid Spot.  I avoided him by blocks.  I was probably in the third grade at the time.  Thus began my life long observations about dogs, dog owners, and their relationship to other people.

Over the intervening decades I have encountered exactly one dog owner who was able to utter the warning: "No - be careful - he bites."  The others usually walk by pretending that nothing is happening as their dog strains to the limits of the leash trying to bite me.  So that is exactly one dog owner with an honest warning as opposed to the tens of thousands who depend on their ability to restrain the dog and protect its reputation?  Help me out here.  Why are dog owners unable to level with people about their dog's real nature?  Would a dog with poorly controlled behavior sully the reputation of the family?

The aggressive nature of dogs should be considered natural instinct.  My scariest incident occurred when I was out cycling one day.  I was out in the country, cycling past farms and silos on a two lane blacktop road with no shoulder.  I had just come up a long hill and was recovering and just starting to pick up speed.  Suddenly I heard four paws hitting the pavement in a rhythmic and rapid manner.  I looked over my shoulder and saw a dog closing in on me.  I recognized the breed immediately but will not type it here.  I have seen the public outcry when dog breeds are named in attack situations and want to avoid that scandal.  I was faced with a very muscular dog torpedo heading right at me.  I was well schooled in what to do about dog attacks having read about it in the cycling literature for decades.  After a fast calculation (fatigue level, strength and conditioning, road surface, incline, current gear, weather conditions)  I decided I could outrun him and after about a quarter of a mile - I did.  I guess even an irrational attacking dog can decide when to give up as the quarry fades on the horizon.

 Humans may be somewhat grandiose in what domestication has accomplished.  Most people saw the recent YouTube video of the dog attack on a toddler and the dog being repelled by the family cat.  What exactly do you think that dog was trying to do?  I have no doubt, but realize that it is too awful for the modern dog owner to contemplate.  Robert Service wrote about it in his poem "The Parson's Son" but I won't quote or link to it from here and encourage only those who can tolerate violent imagery to look it up.  It would be offensive to most dog owners today, many of whom seem to view their dog as a member of the human family.  

Dogs frequently make the news for any number of reasons such as dog attacks, dog abuse,  neglect, and illegal dog fighting but the owners get less press.  Living in the suburbs has provided fertile ground for observing dogs and their owners.  Over half of everybody in my neighborhood owns at least one dog.  Some people own more than two.  In the town where I live there is a leash law and a law that you must pick up your dogs fecal material and dispose of it properly.  Easily half of the dog owners do neither.  The city provides bags and receptacles for collecting this material and places it conveniently at the start of the trail.    The police apparently don't care unless they catch the dog in the act.  Since they are never around there is no chance that will happen.  That has led some of the dog owners to develop somewhat of an outlaw attitude.  That would be exemplified in the following confrontation by a property owner (PO) witnessing a dog defecating on his lawn.  Response by the dog owner are designated (DO).

PO:  "I hope you are going to pick that up."
DO:  "Why it isn't your property."  (The area in question is ten feet from his front door).
PO:  "Actually it is.  What makes you think it is not my front yard."
DO:  "This is the easement and there is supposed to be a public sidewalk here".  (There are no public sidewalks for miles and no easements in the neighborhood).
PO:  "So you do need to pick that up."
DO:  "Well I am not going to."
PO:   "Why not?"
DO:  "Because you're an asshole."

To recap, we have a dog owner here in clear violation of the dog ordinance arguing that the ordinance and property rights can be ignored.  When that argument did not carry the day, an ad hominem attack was initiated.  Clearly at least some dog owners have a strong motivation for their irrational behavior.

A Medline search of dog ownership turned up no references on the rogue behavior of dog owners.  There was research on how dogs affect the physical activity of their owners, the impact of dogs on he immune status of family members at home and even research on the problematic behavior of dogs and how to approach that.  Nothing on the problematic behavior of dog owners.  If there is none, it should be done and I would be very interested in the results.  I am not doubting the positive effects of companionship, the health effects, or the roles of dogs in specific areas of service.  I am more focused on the associated behavior of humans who not only readily dismiss some of the legal responsibilities of dog ownership and expose members of the public who have entirely different experiences with dogs than they do, but also in some situations put dogs at risk.  We are all familiar with the Humane Society ads focusing on neglected and abandoned pets.  The stories about large numbers of neglected dogs are also regular local news fare.  Do those situations result from an unrealistic view of dogs and a serious overestimate about how many dogs one can care for in the first place?  What leads to that bias?

What can be done about the problem?  It seems like a good question for research.  I have seen at least one municipality that does DNA testing of fecal material and compares those results against a mandatory database of DNA samples obtained at the time of licensing.  That level of enforcement seems a bit drastic but compliance with the law seems so low it also makes sense.  Why is it so hard to follow a basic ordinance?  Is the decision to become an outlaw dog owner more similar to the decisions to drive 5 or 10 miles per hour over the speed limit?  Or is it closer to a broker selling you a stock that he and his company are betting against?  Is it as bad as cheating on your taxes and hoping to get away with it?  We may need some neuroeconomists to load some of these folks in an fMRI scanner and see what networks seem to be activated.  I can see the experiment now: "experimental subjects we placed in the fMRI scanner and listened to audio scripts of confrontations about violations of the leash law or collecting dog feces.  Their response was measured...."

Don't get me wrong.  I would never consider "Outlaw dog owner" to be anything like a diagnosis or anything that needs "treatment" .  I would put it in that general class of irrational behaviors that seem to make people miserable and that they seem to be unable to figure out and self correct on their own.  Hence my allusion to Freud's thesis of over a century ago.  As far as I can tell. these dog owners who are otherwise normal and law abiding citizens in most areas of their life are much different with their dog.  Some of my best friends are dog owners.  Dogs seem to be projective tests for a lot of neurotic and otherwise irrational human behavior.  I do think that it speaks to unconscious factors in everyday life that are explained away by overly simplistic observations.   Common approaches are looking at laws and who can abide by them or the fact that some people are "dog lovers" and other are not.  Those factors extend far beyond the realm of dogs, and within that realm there seems to be plenty of unnecessary conflict to go around on any given day.

I have been judged by dog owners for not being affiliative enough with their pets.  I don't throw saliva covered tennis balls or talk to dogs by using baby talk.  I am not a Dog Whisperer, but they all seem to love me - except for Spot.  Maybe because they appreciate the fact that I know their true nature.  At any rate, whenever this happens (the dog jumping excitedly all over me), the owner invariably asks the question about whether or not I want to join the fellowship of dog owners.  I have never owned a dog in my life and don't plan to.  I come up with a lot of excuses, but don't go into a lot of detail.  But occasionally the truth comes out.

I am really a people person.

George Dawson, MD, DFAPA

Supplementary 1:  Outrunning a dog on a bike should only be attempted by a highly skilled cyclist who knows the relevant variables and the other suggested methods for fending off dog attacks.  In a split second you have to weigh the risks of getting caught by the dog as opposed to the relief of getting away.  So do not try this at home.  It is risky even if you have the necessary training and background.  Since this blog is not about cycling, I defer any interested reader to the usual cycling references.

Supplementary 2: The American Academy of Pediatrics has always played a prominent role in educating the public about dogs and children.  They post some incredible statistics on dog bites and the most important and frequently ignored advice about dogs and small children:

"Never leave a baby or small child alone with a dog."