Of Rats and Men

Fear, anxiety, and survival circuits

Brain Circuitry: The Extended Amygdala and Uncertainty

In chapter 4, LeDoux describes the brain circuitry involved in defensive responses to threatening stimuli. In short, the sensory cortex and sensory areas in the thalamus process a threatening stimulus and transmit it to areas in the amygdala which then connect to various areas of the brain leading to defense reactions, increased arousal, and connections to higher-order cortical areas such as the prefrontal cortex and hippocampus (pp. 93, 102, 105).

Most importantly, LeDoux describes a brain area known as the bed nucleus of the stria terminalis (BNST). Also called the extended amygdala, this area of the brain has been shown to process uncertainty (p. 105). The BNST has output destinations similar to those of the amygdala; however, the inputs to the BNST are somewhat different, including input from the prefrontal cortex and the hippocampus, which has a role in memory and relational processing. There are also regions of the BNST that respond to ambiguity.

LeDoux summarizes some of the processes and major brain areas involved when someone is anxiety-ridden: hypervigilance (overactive amygdala); impaired ability to discriminate threat and safety (failure of the prefrontal cortex to regulate the amygdala); increased avoidance (activity in a variety of regions); heightened reactivity to threat uncertainty (increased activity in a variety of areas including the hippocampus and the BNST); overvaluation of threat significance and maladaptive behavioral and cognitive control in the presence of threats (both involve a number of brain areas).

Emergence of Conscious Feelings

Psychoanalysts have been much more interested in the study of unconscious mental activity than in the study of consciousness (Colombo 2008). Yet, as noted in Colombo, some like Wilma Bucci and Bonnie Litowitz stress that the “conscious versus unconscious distinction may not be the most useful one for understanding mental activity and that it may be more fruitful to think in terms of forms of representation that can be used by the mind” (p. 274). For neuroscientists like LeDoux, as well, unconscious or nonconscious processes are much better understood than how conscious subjective experience emerges. As Dresp-Langley and Durup (2009) write, “consciousness studies have produced a considerable bulk of theoretical and experimental works concerned with trying to answer two critical questions: (1) is a scientifically operational definition of consciousness possible and (2) where and how is this phenomenon produced in the brain?” (p. 1). For example, in the “global workspace” ³ model, consciousness is assumed to arise from information captured in working memory and then transmitted to various parts of the brain—“to the language module and be identified and named so that they can be shared with other people, forwarded to the planning module to be reasoned about, and stored in long-term memory if the information is notable enough” (Koch 2014, p. 487). Koch notes that what allows such information to become conscious does not seem to be known.

LeDoux includes a long discussion detailing the controversies regarding the brain mechanisms resulting in consciousness. His primary agenda seems to be understanding the brain mechanisms leading to emotions; how they come to be consciously experience is of secondary interest. He reviews the work of affect theorists dating back to Darwin, focusing mainly on distinguishing his ideas from those of Jaak Panksepp and Antonio Damasio.

LeDoux presents Panksepp as arguing that “powerful emotional feelings result when subcortical emotion command centers are activated in animals and people . . . [and such] basic, subcortical, innate feelings are ‘implicit,’ ‘perhaps truly unconscious,’ and occur ‘without explicit reflective awareness or understanding of what is happening’” (p. 129). LeDoux maintains that “feelings, even primitive ones, have to be felt (consciously experienced)” (p. 129). LeDoux maintains that although his ideas are closer to Damasio’s than to Panksepp’s, Damasio maintains that “feelings are primarily determined by body signals,” whereas he believes that more mechanisms are involved (p. 134). Both Panksepp and Damasio attribute feelings to animals, whereas he does not.

In essence, LeDoux differentiates what he calls “creature consciousness” from “mental state consciousness” (p. 147). Both states of consciousness include being awake and alert; being responsive to sensory stimuli; being able to execute complex behaviors; and being able to solve problems. However, only mental state consciousness includes (1) the awareness that one’s self exists and (2) the awareness that it is one’s self that is sensing, behaving, and solving problems. Throughout his work, LeDoux cites a variety of perspectives comparing the consciousness of animals (other than humans) to human consciousness. He argues that animals demonstrate all the aspects of creature consciousness, but that, regardless of how we personally perceive their responses, the lack of verbal reports makes it impossible to ascertain whether they experience mental state consciousness (pp. 49, 195). He notes Frans de Waal’s comment that although he believes animals have feelings, “we cannot know what they feel” (p. 48). Thus, LeDoux reserves the term consciousness to designate mental state consciousness—in humans, that is.

LeDoux stresses that consciousness so defined depends on cortical processes (p. 175), including the executive function of attention and operation of the mental space of working memory, both central to consciousness. For LeDoux, the connections of subcortical areas with cortical areas are the neural correlates of consciousness, the major areas of this “cortical consciousness network” being the frontal and parietal areas (pp. 178–179). Mark Solms (2013) argues against what he calls the “corticocentric fallacy” regarding consciousness, citing examples of emotional expression in individuals with cortical damage, such as children born with hydranencephaly, a condition in which the cerebral cortex is destroyed in utero. On the other hand, LeDoux, with regard to such a pathological state, argues that “much evidence has demonstrated that malfunctions of brain development can be compensated for [by other areas], and when this happens, all rules are off in terms of what goes where in the brain” (p. 175). In addition, for LeDoux the fact that decortication of animals “does not eliminate purposeful goal-directed activities” may imply not that consciousness is derived from subcortical areas but that “consciousness is not required for goal-directed behavior” (p. 174). Finally, laying no claim to being a consciousness researcher, he “defers to the wisdom of the field to tell us how consciousness comes about. When this is figured out, we will then know how feelings like fear and anxiety come about as well, since they are states of consciousness” (p. 180).

Memory and Consciousness

For the psychoanalyst, chapters 7 and 8 are the heart of this volume: the first deals with how memory affects consciousness, the second with emotional consciousness. LeDoux describes the various kinds of memories: semantic memory refers to memories of factual information; episodic memories refer to stories one has experienced that include a what, where, and when narrative. Both of these are types of explicit or declarative memory; they are consciously accessible and depend on the median temporal lobe memory system. There are also types of implicit memory that are consciously accessible, though not currently conscious: associative conditioning, habits, skills, and priming (p. 190). LeDoux notes that “just as episodic memory depends on semantic memory, semantic and episodic memory both depend on implicit memory. For example, each time we consciously recognize a stimulus, we are drawing upon implicit processes operating in the median temporal lobe memory system. Sensory cues . . . activate a memory via the medial temporal lobe system; then, through a process known as pattern completion, a memory is assembled in a way that can be retrieved into working memory, where it can be consciously experienced” (pp. 190–191).

Thus, although LeDoux mainly stresses that the processes that lead to the retrieval of memories are not consciously available, it does not seem much of a leap to conjecture that memories (such as those contributing to the formation of unconscious fantasies) that are not consciously accessible to the individual (unconscious memories) can be retrieved into consciousness. The fact that priming effects require the activity of the neocortex lends credence to the psychoanalytic hypothesis that such unconscious memories continue to have an effect in the present.

The work of Endel Tulving, discussed by LeDoux, may actually provide evidence for the psychoanalytic hypothesis that the past (memory, whether conscious or unconscious) affects the present. Tulving, who first established the distinction between semantic and episodic memory, described different forms of consciousness. Using the term “noetic” (derived from the Greek word nous meaning mind or consciousness, he distinguished autonoetic consciousness, which allows for the experience of episodic memory, and noetic consciousness, which allows for the experience of semantic memory. LeDoux notes that both semantic and episodic memories are in a preconscious state until retrieved into working memory, which then allows them to be experienced consciously.

Of particular interest from the psychoanalytic perspective, Tulving proposed a third mental state—an anoetic one—that does not occur in conjunction with conscious memories, semantic or episodic. Rather, anoetic states “occur in conjunction with implicit memories, which do not require conscious access for their formation, storage, or retrieval. According to Tulving, anoetic states are triggered automatically (involuntarily), and they remain concealed from consciousness” (p. 193). LeDoux stresses that semantic knowledge can exist in both states, noetic and anoetic alike. “Although conscious semantic memory requires the hippocampus and working memory, and thus reflects noetic consciousness, semantic priming operates nonconsciously and as such is a form of an anoetic [state] that requires neither the hippocampus nor working memory” (p. 193). In my reading, in contrast to his theory that semantic memory may exist in an anoetic state, LeDoux does not say whether he believes that episodic memory can exist in the two forms (autonoetic and anoetic). Can precursors to episodic memory exist in an anoetic conscious state?

Vandekerckhove, Bulnes, and Panksepp (2014) discuss “the emergence of primary anoetic consciousness in episodic memory”: “Anoetic consciousness reflects a primal state of autonomic-phenomenal awakeness, with direct experiences of oneself and the world—namely, an unknowing or ‘anoetic’ (without explicit knowledge) consciousness consisting of perceptual, motoric-procedural and various primal emotional, homeostatic, and sensory affective states” (p. 1). They go on to conjecture that the emergence of episodic memory is guided by anoetic affective consciousness, leading to autonoetic consciousness: “The episodic remembrance of one’s own life experiences is filled with the pervasive affective consciousness associated with specific times, places, and events. It involves a detailed sensory affective-perceptual re-experiencing of events, and this is importantly related to anoetic consciousness. The reliving of the subjective experiences is closely linked to an affective evaluation of the significance of these past experiences for oneself and with respect to one’s previous and present position in the world” (pp. 5–6).

It would seem that such a conception of the significance of anoetic consciousness, if validated, provides a basis for the psychoanalytic concept of “unconscious fantasy” (see, e.g., Arlow 1969; Erreich 2003; Litowitz 2007; Shapiro 2008). If these conjectures about the impact of anoetic consciousness are accurate, can the construct of “unconscious fantasy” as a determinant of current behavior and expressions be understood from the perspective of memory storage? Can one conceptualize unconscious fantasies as implicit memories that emerge from anoetic consciousness and under certain conditions become explicit episodic memories?

Or, in contrast, are the conjectures of the Boston Change Process Study Group (2007) more consistent with neuropsychological memory studies? “Even in a spoken narrative,” they write, “there is meaning between the lines, which is implicit”; they “prioritize implicit forms of knowing and the recognition of action and interaction as part of psychodynamic life because it is in the implicit realm of what happens from moment to moment that affects, conflict and defense become initially organized, later revealed, and potentially changed” (p. 844).

Addressing these complex issues, including the combined impact of emergent explicit episodic memory and implicit forms of knowing, is beyond my scope here, though I will touch on this last in my conclusion.

Emotional Consciousness

Certainly an important issue that memory storage and subsequent retrieval raise for psychoanalysts is whether the perceived event is threatening or emotionally neutral. LeDoux has demonstrated that the amygdala plays a key role in the processing of threat stimuli (pp. 209–211). There are two pathways to the amygdala from the perception (visual, for example) of the potentially threatening stimulus, although both occur nonconsciously. One pathway leads directly from the visual thalamus to the amygdala (the low road); the second leads from the visual thalamus to the visual cortex and only then to the amygdala (the high road). The shorter route allows for quick reaction, whereas the longer allows for a more critical, cortex-based evaluation of the stimulus (again see my stick-in-the-woods example).

LeDoux describes in exquisite detail the various brain areas and pathways involved in the perception of threatening stimuli (whether direct or ambiguous) and the eventual emotional responses. In summary fashion he outlines the steps that occur in the brain in response to a fearful experience (pp. 227–231): (1) representation of a sensory object or event; (2) activation of defensive survival circuits and expression of defense responses and physiological changes (amygdala and extended amygdala); (3) attention ⁴ bringing the stimulus to working memory where conscious awareness takes place (interaction between sensory and prefrontal and parietal circuits); (4) semantic memory with object recognition and discrimination (noetic consciousness involving interaction among cortical areas: sensory, prefrontal, and parietal, working memory circuits, and medial temporal lobe semantic memory circuits); (5) episodic memory (autonoetic state of consciousness).

Step 5 is the most complex of these (and the most important for psychoanalytic theorizing). It not only includes an integration of steps 1–4 but is also dependent on what the individual has learned from personal experience with danger: “Whether you feel concern, alarm, fright, panic, or terror depends on the particular blend of ingredients and the way they are cognitively interpreted via stored schemas. Fear and other emotions are based on assumptions, presuppositions, and expectations; they are constructed in the brain from nonemotional ingredients” (pp. 229–230).

An Exposure/Extinction Model and the Psychoanalytic Process

In his last three chapters, LeDoux discusses a variety of anxiolytic drugs and a number of psychological treatment models, both current and proposed, with a major focus on the use of cognition in exposure therapy to treat fear and anxiety. Exposure therapies rely on the principles of extinction by gradual exposure to Pavlovian-like conditioned stimul:

According to emotional processing theory, the two key factors required for a therapeutic reduction in fear and anxiety are complete activation of the fear structure by fear-arousing stimuli and the insertion of new information into the fear structure that is incompatible with pathological information. . . . new information does not replace old information in the fear structure but instead creates a competing memory that suppresses the old memory. The new memory (new fear structure) lacks the pathological associations that trigger fear and that support and sustain avoidance and prevent extinction; therefore negative emotions (fear and anxiety) and avoidance are reduced [p. 272].

LeDoux notes that for a variety of reasons extinction may be fragile and suggests a variety of methods for making exposure therapy more effective. In addition, he discusses the importance of targeting both explicit and implicit processes. ⁵ Finally, he stresses the importance of promoting active coping mechanisms, say, allowing the rat to control the threatening stimulus by escaping to another cage when threatened or training traumatized individuals to take active steps to avoid freeze-flight-fight reactions (p. 311).

To my knowledge, there are but two articles that consider in detail how the psychoanalytic process may be conceptualized as comparable to the exposure and extinction paradigm of conditioning. Brakel (2011) suggests that “features of classic psychoanalytic technique—the couch, meetings several times a week . . . , and free association—uniquely facilitate intense transferences of various sorts, and that these in turn constitute the multiple and diverse extinction trials necessary to best approximate extinction” (p. 1). Gorman and Roose (2011) write that their

hypothesis, that the process of “working through” in psychoanalysis activates the same anatomical and molecular pathways that conditioning, consolidation, reactivation, and reconsolidation of fear memories do in animals, produces at least two testable predictions: (1) Repetition by the patient of a retrieved traumatic memory should result in some symptomatic improvement according to an extinction mechanism, but this improvement will be tentative and subject to relapse. (2) Psychoanalytic process leading to what is called “structural change” requires the activation of repressed fantasies and the incorporation of reconsolidated versions into new, less toxic unconscious narratives; this should free the patient from the repetition compulsion of neurotic behavior, and this change will be less susceptible to recurrence [pp. 1212–1213].

In our Manual of Regulation-Focused Psychotherapy for Children (RFP-C) for Externalizing Behaviors (Hoffman, Rice, and Prout 2016), we understand that the child’s problematic behaviors should be conceptualized as avoidance mechanisms that offer protection from experiencing unpleasant emotions, such as sadness. Over time, the clinician identifies and addresses this pattern of avoidance, helping the child the child identify these protective, yet maladaptive, coping devices. This then helps the child become able, in time, to discuss the painful emotions themselves. This process of gradual exposure to painful emotions is thus similar to Exposure with Response Prevention (ERP) treatment strategies.

From Defense Survival Circuits to Addressing Defenses in the Clinical Situation (An Experience-Near Intervention)

Throughout the volume, LeDoux notes that he prefers the term nonconscious to unconscious because “the Freudian unconscious is a repository for previously conscious content, a place where anxious thoughts and memories are shipped and kept under wraps; the so-called cognitive unconscious refers to functions that may or may not produce conscious content” (p. 149).

It is crucial to note that the only works by Freud that LeDoux cites (e.g., the 1915 paper on the unconscious) were written before the structural model was introduced. Like many neuroscientists, LeDoux seems to believe that the “Freudian unconscious” refers only to hidden mental content, an idea unfortunately echoed by many psychoanalysts. For example, Mitchell (1998) states that “traditional classical interpretations were regarded purely in semiotic terms, as a decoding, a translation of the manifest meanings of the patient’s associations into latent unconscious meanings” (p. 839). This conception of the “Freudian unconscious” neglects the development of ego psychology, beginning with The Ego and the Id (Freud 1923) and Anna Freud’s The Ego and the Mechanisms of Defense (1936). Contemporary psychoanalytic formulations stress that unconscious mental activity includes processes such as unconscious defense mechanisms (Shapiro 2008; Rice and Hoffman 2014). The idea that the “Freudian unconscious” is simply the repository of unwanted memories is an antiquated construct. Psychological mechanisms too can be unconscious.

This failure to appreciate the importance of addressing a patient’s defenses leads many to believe that psychoanalysts start right in by addressing unconscious mental content, such as unconscious fantasy. LeDoux, Mitchell, and others would seem to believe that when a patient expresses a symptom (a pathological response to some threatening object, event, or internal experience) the analyst very quickly intervenes at the level of semantic or episodic memory (steps 4 or 5 as outlined above), entirely bypassing the earlier stages. This view would have the analyst addressing the purported meaning of the patient’s symptomatic acts, either with a symbolic interpretation addressing semantic memory (noetic consciousness) or by quickly positing the impact of an event from the patient’s past (episodic memory, autonoetic consciousness) on the present.

In reality, however, most analysts would first address steps 1 or 2, which involve defensive processes, an approach that has been conceptualized as starting with the “analytic surface” (see Levy and Inderbitzin 1990). By staying at the analytic surface the analyst remains in an experience-near mode, without having to guess the connection of present symptoms with past events (which may be in anoetic consciousness). For example, Paul Gray (1973) provides a clinical example of staying in an experience-near mode (showing the patient what is happening in the here and now of the session—addressing level 3, how his attention shifted) rather than in an experience-distant mode (cognitively addressing a repetitive pattern in his life—addressing level 5, connecting his present situation to something in his past): “take a patient who refers to some clearly competitive situation and then expresses some passive form of response to it. It may be valid to point out to the patient that he characteristically deals this way with competition in his life. On the other hand, if he can be shown that the passive trend he adopted while talking about the particular situation represented a form of defense at that moment, he will be in a better position to work toward analytic changes of such character traits” (pp. 477–478).

More recently, Lotterman (2012) has noted that in contrast to ideas and fantasies, affect “is an especially good marker of the workable psychic surface. Affect is part of a very early signaling system that alerts the individual and others about the status of the self. It is a rapid response and a largely automatic reaction that is only partially controlled by the ego and its defenses. Affects by their very presence mark the fact that a certain mental element has become significant to the self; therefore, affect can be a particularly consistent and helpful barometer of what is currently on the patient’s mind” (p. 330; emphasis added).

Such experience-near techniques, throughout the analytic or psychotherapeutic work, can help integrate psychoanalytically informed treatments with contemporary neuroscience as described by LeDoux.

Conclusion

LeDoux describes the use of cognitive techniques, in addition to exposure therapy and desensitization, including distraction or proactive temporary avoidance to deal with threatening situations (e.g., a room full of strangers at a party). These techniques use explicit top-down emotion regulation mechanisms while addressing step 3.

Bucci (2011), from the perspective of her Multiple Code Theory, suggests the term avoidant dissociation (in contrast to adaptive dissociation) to characterize the psychological shifts that occur when patients experience threatening ideas. This psychological mechanism occurs in people with emotional disturbances deployed to avoid threatening stimuli so that “integration of new information and flexibility of response is blocked” (p. 252). She notes that there are two varieties of avoidant dissociation: primary and secondary. Primary dissociation (resulting in an almost total inability to integrate physiological and psychological responses) occurs when a trauma is severe. In secondary dissociation, the result of less severe trauma, the physiological effects are less intense but the defense of turning away from threatening stimuli persists.

In sticking with the analytic surface, the analyst or therapist addresses the patient’s defensive avoidance directly, providing an implicit emotion regulation communication. As Gray noted, the patient is “shown that the passive trend he adopted while talking about the particular situation represented a form of defense at that moment.” In other words, the patient is made aware that he has unconsciously directed his attention away from a threatening idea (step 3). It is, of course, difficult to know the impact of the words spoken by the analyst, in contrast to (or in conjunction with) the importance of the message between the lines as described by the Boston Change Process Study Group. This idea of defensive avoidance is consistent with Bucci’s.

Finally, in our work we focus on the therapeutic value of addressing a child’s defenses against unpleasant affects in an experience-near way (Hoffman, Rice, and Prout 2016). It remains to be seen whether it is clinically more advantageous to continue using the term defense against unpleasant affect or more helpful to use LeDoux’s concept focusing on the child’s defensive responses to a threatening stimulus.

In short, clinicians, cognitive scientists, and and experimental neuroscientist seem to agree that a key element in the treatment of patients is helping them address how they turn away from disturbing stimuli in the here and now, and helping them develop more adaptive ways of mastering threatening stimuli.

For that reason alone, LeDoux’s ideas are to be studied and mastered.