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Psychoanalytic Theory: Clues from the Brain:Commentary by Joseph LeDoux (New York)Joseph LeDouxa

a Center for Neural Science, New York University, 4 Washington Place, New York, NY10003, e-mail:Published online: 09 Jan 2014.

To cite this article: Joseph LeDoux (1999) Psychoanalytic Theory: Clues from the Brain: Commentary by Joseph LeDoux(New York), Neuropsychoanalysis: An Interdisciplinary Journal for Psychoanalysis and the Neurosciences, 1:1, 44-49, DOI:10.1080/15294145.1999.10773244

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pointed role of verbally communicating with others."Where does that stop?

I shall now end by saying a few words on theway I think Freud should be read. Freud has no specialright to be considered as telling the truth more thanhis followers who may disagree with him. But in myopinion, Freud has considerable theoretical consis­tency, stronger than any other, even if this is now putto question. What I recommend is to study his workby trying to grasp this internal consistency more thanby considering the isolated facts to which he drewattention. This to me is true rigor, instead of hastilytrying to find impossible compromises between incom­patible methods. For instance, affects in his work aremainly considered first in relationship with represen­tations and then in connection with instinctual im­pulses and the unconscious ego. As far as I know, onlyDamasio seems to bother about the relationship of af­fects to representation.

What psychoanalysts expect from their dialoguewith neurobiologists is not an accumulation of refer­ences related to localization circuits or the effect ofchemical substances, but help in understanding thegeneral patterns of brain functioning. Not that it will

Psychoanalytic Theory: Clues from the BrainCommentary by Joseph LeDoux (New York)

Introduction

Psychoanalytic theory has influenced contemporaryWestern culture in innumerable ways. Although I havenever actually tested aspects of psychoanalytic theoryin my research on emotions and the brain, "psychoan­alytic-like" concepts (such as the unconscious, affect,and emotional memory) have been key to the way Ihave interpreted my research findings over the years(LeDoux, 1996). I refer to these as "psychoanalytic­like" because I don't have a deep understanding ofpsychoanalytic theory and have borrowed the conceptsmore from popular culture (films, novels, and justplain common knowledge) than from Freud's writings.

Acknowledgments: Supported by PHS Grants, MH46516, MH38773,and MH00956, and by a grant from the W.M. Keck Foundation toNYU.

Joseph LeDoux, Ph.D., is Professor, Center for Neural Science, NewYork University.

Joseph LeDoux

change so much their ways of working (i.e., analyzing)but it may broaden their views and satisfy their curios­ity, if they have any, on the topic that will alwaysremain of interest to them: the brain-mind problem.

References

Edelman, G. (1992), Bright Air, Brilliant Fire. New York:Basic Books.

Freud, S. (1900), The Interpretation of Dreams. StandardEdition, 5. London: Hogarth Press, 1953.

--- (1940), An Outline of Psycho-Analysis. StandardEdition, 23:139-207. London: Hogarth Press, 1964.

Moruzzi, G., & Magoun, H. (1969), Brain stem reticularformation and activation of the EEG. Electroenceph.Clin. Neurophysiol., 106:371-392.

Stern, D. (1985), The Interpersonal World of the HumanInfant. New York: Basic Books.

Andre Green9 Avenue de L'Observatoire75006 ParisFrancee-mail: andregreen@compuserve.com

From time to time, I've looked through books by Freudfor research inspiration, but I never found my experi­mental muse there. Lacking the training and contextin which to really understand Freud, I don't think Iever got beyond the surface notions that most collegeeducated people are familiar with. Consequently, thearticle by Solms and Nersessian has done me, andperhaps other neuroscientists, a great service. Al­though I have still not found experimental inspirationin psychoanalytic theory, I feel that I now understandthe theory of affect a little and am grateful for theirtranslation of the theory in terms that are intelligibleto those of us who are not trained in the area. Below,I am going to comment on several points made bySolms and Nersessian in order to do my own transla­tion of some of their notions in terms related to mod­ern work on the brain mechanisms of emotion andcognition. I'll also comment briefly on Panksepp'sdiscussion of their paper.

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Commentary on Emotions: Neuro-Psychoanalytic Views 45

The "Pleasure Principle" Meets CognitiveScience

Solms and Nersessian elaborate on Freud's "pleasureprinciple." This staple of psychoanalytic theory isvery close conceptually to the "law of effect," a no­tion proposed by Thorndike in the early twentieth cen­tury to explain how learning occurs (Thorndike,1913). According to the "law" those behaviors thatare followed by reward are stamped in and those fol­lowed by punishment are stamped out. The "law"played an important role in learning theory, whichformed the core of early experimental psychology.The legendary historian of psychology, E. G. Boring,pointed out that the "principle" and the "law" have ahistorical connection to Jeremy Bentham's eighteenthcentury theory of "hedonism," but each with its owntwist: Thorndike's "law" was a hedonism based onpast events, whereas Freud's "principle" was a hedo­nism based on future expectations (Boring, 1950).

What is interesting is that the two major traditionsin psychology, the clinical and the experimental, havehedonism as a common theme in their history. Al­though often completely separated today, these twobasic approaches to the ways in which mental/behav­ioral functions operate may in the end not be so differ­ent at the core, or at least there may be a fundamentalcommon core to clinical and experimental psychologythat can be used as a conceptual bridge between psy­choanalysis and neuroscience. Modern neuroscience isclosely allied with and compatible with experimentalpsychology, but conceptually is miles away from psy­choanalytic theory. If experimental psychology andpsychoanalytic theory can be fused, even somewhat,the translation of psychoanalytic concepts into brainmechanisms might be achieved in steps, and less pain­fully.

Of course, Dollard and Miller (1950) took a stabat translating psychoanalysis into experimental psy­chology terms in the 1950s. In the meantime, though,experimental psychology was completely overhauledby the cognitive revolution (Gardner, 1987). As a re­sult, the contribution of Dollard and Miller, while stillimmensely interesting, is itself in need of a translationinto modern, especially cognitive, terms. Matt Erdelyimade an effort in the 1980s to translate psychoanalysisinto cognitive psychology in his book, Psychoanaly­sis: Freud's Cognitive Psychology (1985), but as faras I know not much has happened since.

One benefit of the cognitive revolution was thedevelopment of a rich new understanding of how cer­tain aspects of the mind, like perception, attention, and

memory, work. Another benefit was that the uncon­scious (in this case the cognitive unconscious ratherthan the repressed unconscious of psychoanalytic the­ory) became a scientifically legitimate concept withbroad acceptance (Kihlstrom, 1987). On the otherhand, a major drawback of the cognitive revolutionwas that topics like emotion and motivation, and evenlearning, were largely ignored. The law of effect, forexample, plays little role in cognitive theories of howmemories are created. Over the last couple of years,though, the shortsightedness of cognitive theory hasbeen receding, with cognitive scientists becomingmore and more interested in how emotions and cogni­tion relate and interact.

It seems to me that we are poised for a new ap­proach to the mind, one that could embrace theoriesof emotion and personality, learning theory, cognitiveconcepts, and even psychoanalytic notions, in an ef­fort to understand how our brains make us who weare. Some have proposed an "affective neuroscience"as an antidote to cognitive science. My preference isfor a nonpartisan "mind science" that embraces emo­tion and cognition (and other facets of the mind) onneutral ground.

Feelings as the Conscious Perception ofSomething Unconscious

Modern ideas about consciousness coming out of neu­roscience (and cognitive science) often assume thatworking memory is a staging area for consciousness,a network in the brain that can represent the stuff weare aware of when we are aware of something (seeKihlstrom, 1987; Johnson-Laird, 1988; Baars, 1988;Dennett, 1991; Kosslyn and Koenig, 1992; LeDoux,1996). Freud's notion, described by Solms and Ners­essian, that "felt emotions are a conscious perceptionof something-something which is, in itself, uncon­scious," is compatible with the working memoryconcept.

For example, we now know that the amygdala isan important component of the brain system that de­tects and responds to danger. However, the amygdalais not directly responsible for conscious feelings offear. Building on the working memory notion, I haveproposed that conscious feelings of fear come aboutwhen working memory is occupied with the fact thatthe amygdala has detected and begun to respond todanger (see LeDoux, 1996). The amygdala does thesethings implicitly, which is to say unconsciously. Whenworking memory becomes occupied with the fact that

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the amygdala is active (either by direct connectionsfrom the amygdala to cortical areas, by way of connec­tions from the amygdala to brain stem areas that thenflood the cortex with nonspecific neurochemical mes­sages, or by way of connections from the amygdalato areas controlling peripheral responses that thenfeedback to the brain), then we have some of the ingre­dients that turn an experience into a fearful experi­ence. Working memory is also able to represent, atthe same time, the perceptual nature of the externalstimulus as well as long-term memories that have beenactivated by this stimulus. So the immediate stimulus,plus the memories it activates, and the fact that theamygdala has been set into action, all combine to giverise to the feeling of being afraid. When electricalstimuli applied to the amygdala of humans elicit feel­ings of fear (see Gloor, 1992), it is not because theamygdala "feels" fear, but instead because the vari­0us networks that the amygdala activates ultimatelyprovide working memory with inputs that are labeledas fear. This is all compatible with the Freudian notionthat conscious emotion is the awareness of somethingthat is basically unconscious.

Where modern neuroscience might diverge a bitwith the Freudian notion is on the topic of whetheraffect is a separate modality of consciousness. As de­scribed above, I believe we have one basic mechanism(the working memory networks) for representing con­sciousness content. Consciousness (working memory)can be occupied with mundane or significant events,depending on the system that is controlling the occupa­tion. Emotional states of consciousness tend to bemore prolonged and intense because of the greatervariety of brain systems that are called into play tocontribute in various ways to working memory. Theseadditional systems, like brain stem neurochemical sys­tems and peripheral feedback from bodily responses,including hormonal feedback, help lock us into thestate we are in and ensure that our perceptions, atten­tions, and memories stay focused on the significantevent and make it harder for other things to bump thisevent out of working memory. At the same time, re­cent data suggesting that working memory is possiblymade up of multiple overlapping networks, some ofwhich have better connectivity with the amygdala andother subcortical areas, suggests there could be someaffective compartmentalization in working memorythat could constitute something like a modality for af­fective consciousness (LeDoux, 1996). However,much more work is needed on this topic.

Joseph LeDoux

Quantity vs. Quality of Excitation

Solms and Nersessian raise this issue and rightly pointto the long-standing distinction between specific andnonspecific systems in the brain. There have beenmany versions of this notion, but most of them go backto the concept of the sensory systems being involved inrepresenting qualities (objects) in the world, and thereticular formation being involved in nonspecific acti­vation or arousal elicited by those objects. The ques­tion has always been, What arouses arousal systems?How, in other words, does the reticular formationknow that a particular stimulus with a past history ofcausing harm is dangerous, but one very similar to itbut without the history is safe? The fact is that to"know" about stimuli requires that the forebrainsomehow gets in the act. A great deal of work hasshown that the detection of danger is done by theamygdala, on the basis of specific sensory inputs fromthe thalamus and cortex. The thalamus and cortex in­form the amygdala about features of objects or evenabout whole objects. If these features or whole objectshave been "conditioned" by past experiences, theamygdala will respond. Once the amygdala responds,it broadcasts to the cortex, to brain stem areas thatcontrol bodily responses, and to brain stem reticularformation arousal areas that then activate the forebrain(including the amygdala, cortex, and other areas). Inthis view, the amygdala is presynaptic to the reticularformation in the triggering of nonspecific arousal. Thesensory systems and their representations in the thala­mus and cortex provide the amygdala with "quality"and the amygdala, by way of triggering the brain stem,participates in the generation of ' 'quantity. ' , Ofcourse, for the creation of a conscious emotional expe­rience with quantity and quality we need to then turnback to the notion of working memory, elaboratedabove. In this sense working memory evaluates thepresent stimulus situation in light of the fact that thefear system has been activated and is producing certainphysiological responses in the brain and body.

Inhibition and Affective Taming

Just how the brain brings emotional responses undercontrol has long been an important question. Fromthe time of Henry Head (1921) onwards, it has beenbelieved that the cortex somehow inhibits subcorticalregions, and cortical inhibition of subcortical struc­tures plays some role in the regulation of our emo­tional reactions. Adapting Plato's metaphor, the cortex

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Commentary on Emotions: Neuro-Psychoanalytic Views 47

would be the charioteer (reason) that reins in the wildhorses (subcortical emotional systems). Many haveproposed, from clinical observation, that the frontalcortex might be especially involved in this kind ofinhibition. In studies of rats aimed at understandinghow learned fear is extinguished, we found evidenceconsistent with this view (Morgan, Romanski, andLeDoux, 1993). In brief, when the medial prefrontalcortex (anterior cingulate/infralimbic region) wasdamaged the rats took much longer to extinguish theirfear reactions. This suggests that the medial prefrontalregion might normally be involved in regulating theamygdala and the fear reactions it controls (connec­tions from the medial cortex to the amygdala make thissuggestion plausible anatomically). When the medialprefrontal region is damaged, the control is lost, andthe fear remains unchecked. There are several implica­tions of this. One is that it is possible that there arealterations in the medial prefrontal region of somepeople who have difficulty bringing their fears andanxieties under control. A second implication is thatextinction is sort of like behavioral therapy (desensiti­zation). If the medial cortex is involved in desensitiza­tion, it would explain why behavior therapy workswell for simple fears (connections from the medialcortex to the amygdala make it possible for desensiti­zation to reduce fear reactions).

It is interesting to speculate that talking therapyinvolves other parts of the cortex, namely the lateralprefrontal cortex, which is crucially involved in work­ing memory (Fuster, 1989; Goldman-Rakic, 1993). Tothe extent that thinking and reasoning, and especiallyconscious awareness of one's thoughts, involve work­ing memory, working memory networks of the lateralprefrontal cortex might playa key role in talking ther­apy. However, the connections of the lateral prefrontalcortex, with the amygdala, in contrast to the medialprefrontal cortex, are meager and indirect. This mayaccount at least in part for why talking therapy gener­ally takes longer to achieve effects than extinction ap­proaches. But time is not the only consideration sincedesensitization does not work for everything. And if,as speculated above, people with uncontrollable fearhave alterations in the medial prefrontal cortex, it maybe that the best psychotherapeutic hope for them is inthe form of talking cures.

Repression, Stress, and Multiple MemorySystems

The notion of repression is central to psychoanalytictheory. Modern neuroscience has provided an alterna-

tive explanation that might account for some of whathas been called repression. I am not proposing thatrepression is an invalid concept, but only that thisother explanation should be ruled out when repressionis considered to be involved.

The key to our conscious memories is a networkin the medial temporal lobe involving the hippocampusand related brain regions (see Squire, Knowlton, andMusen, 1993; Cohen and Eichenbaum, 1993; Milner,Squire, and Kandel, 1997). It is now known that stress(by way of adrenal steroid hormones) adversely af­fects the function of the hippocampus (McEwen andSapolsky, 1995). Thus, it is possible that in periods ofintense stress the hippocampus is in effect shut down,or impaired, to the point of being unable to perform thenormal functions that create memories. Thus, amnesiaafter being raped or mugged might have as much todo with the adrenal shut down of the hippocampus aswith the shunting of unpleasant memories from con­sciousness. One might even go out on a limb and at­tempt to explain repression in biological terms, but atthis point it may be best to keep these notions separate.

But how can the effects of stress continue to af­fect the traumatized person if the stress interfered withthe ability to store the experience? The answer comesin the form of multiple memory systems. We nowknow that there are many kinds of memory, each me­diated by different brain systems (see Squire et aI.,1993; Cohen and Eichenbaum, 1993; LeDoux, 1996;Milner et al. 1997). The two of interest to this discus­sion are the medial temporal lobe system, which medi­ates our conscious or explicit memories, and theamygdala, which is involved in implicit (unconscious)storage of memories about harmful situations. Andwhile stress impairs the functions of the hippocampus,it seems to amplify the functions of the amygdala (fordiscussion see LeDoux, 1996). So the exact conditionsthat might lead one to have an amnesia (loss of con­scious memory) for the events surrounding a traumaticevent, might also lead to a particularly powerful un­conscious memory that has direct influence on the waythe person acts and feels. Because these influences areoperating unconsciously, the person would have littleunderstanding of why the actions or feelings occur.

Panksepp's Consilience

Panksepp's detailed discussion of Solms and Nerses­sian provides a valuable aid to those seeking to linkneuroscience and psychoanalysis. However, I do take

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issue with some of Panksepp's basic assumptionsand conclusions.

Let me first point out that Panksepp's idea ofemotional command systems is very important anduseful. From a purely conceptual point of view itseems likely that if emotions are survival functionsthen different emotions should have different neuralunderpinnings. The logic here is simple: Since differ­ent aspects of survival are achieved by different kindsof behavioral responses and these require differentneural control networks that are called upon in differ­ent situations, then different neural systems might verywell be involved. My work has concentrated on thefear or defense system, which we have mapped out insome detail (LeDoux, 1996). However, others, includ­ing Panksepp, have collected data suggesting that dif­ferent emotions involve different (at least somewhatdifferent) brain systems.

I part with Panksepp on the implications of thefindings. He proposes that since the command net­works are the same in humans and other animals, thenthe subjective states experienced should be the same.That is, activation of the fear command system shouldproduce similar feelings of fear in people and othermammals (and perhaps other animals as well). This isof course possible. However, as outlined above, myview of subjective feelings is that they involve therepresentation in working memory of the activity ofunconsciously operating systems (like the emotionalcommand systems that Panksepp talks about). In thissense, the conscious experience of being in danger (the'feeling of being afraid) is mediated in the same wayas the conscious experience that an apple is red. Thedifference is that the fear experience involves morebrain and body systems. The reason emotions feel dif­ferent from nonemotions, in this view, is because ofthese additional inputs to working memory: They addintensity and duration to emotional states, whichwould otherwise disappear from consciousness assoon as something else comes along. If we are in thethroes of danger, or rapt in love, it makes good sense(from the point of view of survival) to maintain thosestates unless something more important comes along.

In general, Panksepp and I seem to disagree at afundamental level about what behavioral data can re­veal about an animal's brain. Can we say that becauserats and people respond the same way in situations ofdanger or play, that fear or joy that a person experi­ences is also experienced by the rat? Panksepp saysyes. I say there is no way to know. This is not exactlythe same as the philosophical problem of other minds,which asks how can I know if anyone other than me

Joseph LeDoux

is conscious. At least with other people we can drawupon the fact that we all have basically the same kindsof brains and may therefore have the same kinds ofmental states. But when it comes to making such com­parisons across species, where the brains differ sig­nificantly, at least in terms of the neocortex, we facevery difficult problems. These problems are com­pounded by the fact that the prefrontal cortex, whichcontains the working memory networks and thereforeis believed to be involved in human conscious experi­ence, is the region the differs most between humanand other brains. For these reasons, when I think aboutemotion as a subjective conscious feeling, I prefer torestrict my theorizing to human brains.

Conclusion

We are far from bridging psychoanalysis and neurosci­ence. However, Solms and Nersessian have provideda very nice launching pad for this endeavor.

References

Baars, B. J. (1998), A Cognitive Theory of Consciousness.New York: Cambridge University Press.

Boring, E. G. (1950), A History of Experimental Psychol­ogy. New York: Appleton-Century-Crofts.

Cohen, N. J., & Eichenbaum, H. (1993), Memory, Amnesia,and the Hippocampal System. Cambridge, MA: MITPress.

Dennett, D. C. (1991), Consciousness Explained. Boston:Little, Brown.

Dollard, J. C., & Miller, N. E. (1950), Personality and Psy­chotherapy. New York: McGraw-Hill.

Erdelyi, M. H. (1984), The recovery of unconscious (inac­cessible) memories: Laboratory studies of hypermnesia:In: The Psychology of Learning and Motivation: Ad­vances in Research and Theory. New York: AcademicPress, pp. 95-127.

Fuster, J. M. (1989), The Prefrontal Cortex. New York:Raven.

Gardner, H. (1987), The Mind's New Science: A History ofthe Cognitive Revolution. New York: Basic Books.

Gloor, P. (1992), Role of the amygdala in temporal lobeepilepsy. In: The Amygdala: Neurobiological Aspects ofEmotion, Memory, and Mental Dysfunction, ed. J. P. Ag­gleton. New York: Wiley-Liss, pp. 505-538.

Goldman-Rakic, P. S. (1993), Working memory and themind. In: Mind and Brain: Readings from ScientificAmerican Magazine. New York: W. H. Freeman, pp.66-77.

Head, H. (1921), Release function in the nervous system.Proc. Roy. Soc. Lond. BioI., 92B:184-187.

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Commentary on Emotions: Neuro-Psychoanalytic Views 49

Johnson-Laird, P. N. (1988), The Computer and the Mind:An Introduction to Cognitive Science. Cambridge, MA:Harvard University Press.

Kihlstrom, J. F. (1987), The cognitive unconscious. Science,237: 1445-1452.

Kosslyn, S. M., & Koenig, O. (1992), Wet Mind: The NewCognitive Neuroscience. New York: Macmillan.

LeDoux, J. E. (1996), The Emotional Brain: The MysteriousUnderpinnings of Emotional Life. New York: Simon &Schuster.

McEwen, B. S., & Sapolsky, R. M. (1995), Stress and cog­nitive function. Curro Opinion in Neurobiol., 5:205-216.

Milner, B., Squire, L. R., & Kandel, E. R. (1998), Cognitiveneuroscience and the study of memory. Neuron,20:445-468.

Commentary by Allan N. Schore (Los Angeles)

Over the last two decades, Freud's seminal model ofa dynamic, continuously active unconscious mind hasundergone a major transformation. Yet most disci­plines that border psychoanalysis, "the science of un­conscious processes," are unaware of these importantadvances. A rapidly evolving trend within contempo­rary psychoanalysis, at both the levels of theory andpractice, is an increasing appreciation of the centralityof affective phenomena. Freud first delineated hisideas about affect in 1895 in the "Project for a Scien­tific Psychology," an attempt to create a systematicmodel of the functioning of the human mind in termsof its underlying neurobiological mechanisms (Schore,1997a). Although he subsequently contended that thework of psychotherapy is always concerned with af­fect (1915), it is only recently that an increased em­phasis on affect is impacting clinical models.

In this same time frame, after a long period ofneglect, the other biological sciences have begun toearnestly explore the problem of emotion. As the firstissue of this important journal demonstrates, affectand its regulation are a potential convergence point ofpsychoanalysis and neuroscience. In the following Iwill briefly comment upon Solms and Nersessian'sand Panksepp's essays, and then, utilizing an interdis­ciplinary perspective, offer some ideas about affectand its development. Throughout my commentaries, I

Allan N. Schore, Ph.D., is Assistant Clinical Professor, University ofCalifornia at Los Angeles School of Medicine; and Faculty, Institute ofContemporary Psychoanalysis, Los Angeles.

Morgan, M. A., Romanski, L. M., & LeDoux, J. E. (1993),Extinction of emotional learning: Contribution of medialprefrontal cortex. Neurosc. Letters, 163: 109-113.

Squire, L. R., Knowlton, B., & Musen, G. (1993), The struc­ture and organization of memory. Ann. Rev. PsychoI. ,44:453-495.

Thorndike, E. L. (1913), The Psychology ofLearning. NewYork: Teachers College Press.

Joseph LeDouxCenter for Neural ScienceNew York University4 Washington PlaceNew York, NY 10003e-mail: ledoux@cns.nyu.edu

will argue that a common ground of both psychoanaly­sis and neuroscience lies in a more detailed chartingof the unique structure-function relationships of theright brain, which Ornstein (1997) calls "the rightmind." Psychoanalysis has been interested in the righthemisphere since the split brain studies of the 1970s,when a number of psychoanalytic investigators beganto map out its preeminent role in unconscious pro­cesses (Galin, 1974; Hoppe, 1977). I will suggest thatFreud's affect theory describes a structural system, as­sociated with unconscious primary process affect­laden cognition and regulated by the pleasure-unplea­sure principle, that is organized in the right brain.

A Perspective from Classical Psychoanalysis

In their concise presentation of Freud's theory of af­fect Solms and Nersessian underscore his ideas that"basic emotions" are forged in early development,and that in later life they represent "reproductions ofvery early experiences of vital importance" to notonly the "individual but of the species" (Freud1916-1917). There is now an intense interest in "bio­logically primitive emotions" which are evolution­arily very old, appear early in development, and arefacially expressed. The early maturing right hemi­sphere is dominant for the first three years of life(Chiron, Jambaque, Nabbout, Lounes, Syrota, and Du­lac, 1997), and it contains a basic primitive affect sys­tem (Gazzaniga, 1985) that is involved in the

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