The default-mode, ego-functions and free-energy: a neurobiological account of Freudian ideas

This theory-building paper (2010) attempts to provide models of neural substrates for a variety of Freudian hypothetical constructs.

Abstract

“This article explores the notion that Freudian constructs may have neurobiological substrates. Specifically, we propose that Freud’s descriptions of the primary and secondary processes are consistent with self-organized activity in hierarchical cortical systems and that his descriptions of the ego are consistent with the functions of the default-mode and its reciprocal exchanges with subordinate brain systems. This neurobiological account rests on a view of the brain as a hierarchical inference or Helmholtz machine. In this view, large-scale intrinsic networks occupy supraordinate levels of hierarchical brain systems that try to optimize their representation of the sensorium. This optimization has been formulated as minimizing a free-energy; a process that is formally similar to the treatment of energy in Freudian formulations. We substantiate this synthesis by showing that Freud’s descriptions of the primary process are consistent with the phenomenology and neurophysiology of rapid eye movement sleep, the early and acute psychotic state, the aura of temporal lobe epilepsy and hallucinogenic drug states.”

Authors: Robin L. Carhart-Harris & Karl J. Friston

Summary

Introduction

We explore the notion that Freudian constructs may have real neurobiological substrates, and that they can be usefully revisited in the context of modern neuroscience. We show that the psychoanalytic distinction between the primary and secondary processes fits comfortably with modern notions of functional brain architecture.

We will discuss the construct validity of Freudian concepts, the Helmholtzian brain framework and empirical findings from neuroimaging to enable a dialogue between psychoanalysts and neurobiologists.

The primary and secondary process

Freud came to the realization that there are two fundamentally different modes of cognition through a study of ‘altered’ or ‘non-ordinary’ states of consciousness. He named these modes the primary and secondary processes, and defined the secondary process as one of converting ‘free energy’ into ‘bound energy’.

We can say that nervous or psychical energy occurs in two forms, one freely mobile and another, by comparison, bound. The primary process is the one that governs the course of events in the ego, while the secondary process controls the unconscious.

Free-energy and the Bayesian brain

Helmholtz’s suggestion that the brain is an inference machine is now a fundamental premise in neurobiology. The free-energy principle is a measure of surprise that is used routinely in modelling empirical data and in neuronal simulations of perception and action.

The brain constructs its own top-down prior expectations about sensory samples from the world, and uses a hierarchy to represent this information. This hierarchy is reflected in the temporal extent of what is represented.

The hierarchical architecture may accommodate the distinction between the Freudian primary and secondary processes, where the secondary process provides top-down predictions to reduce free-energy associated with the primary process.

Intrinsic brain networks and the default mode

During unconstrained ‘resting’ states, the blood oxygen level dependent (BOLD) signal of functional magnetic resonance imaging (fMRI) shows spontaneous fluctuations. These fluctuations identify large-scale intrinsic networks, including the default-mode network (DMN), which is functionally and structurally connected. In this article, we pursue the idea that intrinsic networks function to suppress prediction errors at lower levels, and that failures of top-down control are associated with non-ordinary states of consciousness.

This article discusses how the DMN regulates endogenous excitation and suppresses exogenous stimuli, and how a loss of top-down control over limbic activity is equivalent to a loss of ego control over the primary process.

Large-scale intrinsic networks, the secondary process and ego

Freud’s account of the ego in the Project for a Scientific Psychology introduces the idea that the ego is an organization that receives and contains/represses bottom-up endogenous excitation.

The secondary process is the mode of cognition of the ego, and is ‘inhibited’ and ‘bound’ in contradistinction to the primary process, which is ‘free’ and ‘motile’. The primary and secondary processes owe their inception to observations of non-ordinary states of consciousness.

Functional anatomy of the default-mode

A high-level distributed system whose activity is reciprocally related to the activity in cortical areas subserving task or stimulus-bound processing was identified by Marcus Raichle in 2001. This network is associated with phenomena such as self-referential processing, autobiographical recollection, mind-wandering and theory-of-mind.

The DMN is made up of the medial prefrontal cortex, the posterior cingulate cortex, the inferior parietal lobule, the lateral and inferior temporal cortex and the medial temporal lobes. It develops through ontogeny, in a manner that parallels the emergence of ego-functions.

Model and data-driven analyses suggest that the medial temporal lobes are connected to the medial prefrontal cortex and posterior cingulate cortex nodes of the dorsolateral prefrontal network (DMN), and that this connectivity increases through ontogeny with a notable increase at puberty.

There is a huge amount of evidence supporting the limbic-suppressive function of the medial prefrontal cortex, including correlations between primitive thought and emotion and the medial prefrontal cortex, as well as between the recollection of distressing memories and emotions in patients with post-traumatic stress disorder and the medial prefrontal cortex. The medial prefrontal cortex sends dense projections to the ventral striatum and midbrain, and the ventral striatum and midbrain signal prediction-error and motivational-salience. The DMN comprises high-level cortical nodes that exchange neuronal signals with subcortical systems.

Theoretical formulations of the default mode

Freud argued that the ego modulates both endogenous and exogenous excitation, and that healthy, adult waking cognition depends on the formation of an equilibrium between the pressing forces of the primary process (entailed by the id) and the counter forces of the secondary process (entailed by the ego).

Forward connections originate in the supragranular layers and terminate in layer four spiny stellate cells. Backward connections are more abundant and diffuse and target lower cortical areas. Based on Bayesian and Helmholtzian principles, it has been proposed that forward connections convey prediction-errors that optimize representations in higher levels. These predictions are then used to form predictions that suppress or cancel prediction-errors in lower levels, until they can be minimized no further.

The principle that governs all mental processes is Fechner’s tendency towards stability, and the mental apparatus is designed to reduce excitation.

Freud cited Gustav Fechner as his inspiration for these ideas, because the brain explicitly encodes prediction-error with neuronal activity that is suppressed or explained by backward afferents.

Freud argued that the ego modulates and suppresses both exogenous and endogenous signals. Exogenous signals correspond to sensory signals from thalamic and unimodal areas, and endogenous signals correspond to bottom-up prediction errors.

The DMN suppresses limbic and paralimbic activity and this is associated with the suppression of endogenous activity by the ego.

Hierarchical brain systems

The dorsolateral prefrontal cortex, the dorsal anterior cingulate cortex, the frontal eye fields, the extrastriate cortex, the superior parietal lobule, the intraparietal sulcus and the ventral premotor cortex are associated with the attention system, which is activated during externally-directed cognition and deactivated during internally-directed cognition.

Recent work has suggested that the attention system is not a unified system, but is instead divided into a salience system and a dorsal attention system. These systems are not well integrated with each other.

Under a Helmholtzian model, the DMN is at the top of the hierarchy, and the salience and dorsal attention systems are at intermediate levels, above thalamic and unimodal sensory cortex. These systems self-organize through recurrent message-passing.

Spontaneous BOLD oscillations and neuronal activity

Recent work has shown that spontaneous BOLD-signal oscillations are most probably generated by neuronal activity and that they correlate with spontaneous neuronal fluctuations in multi-unit firing rates and local field potential gamma power. These fluctuations are coherent across the hemispheres and may reflect cortical coherence associated with secondary process cognition.

In general, oscillatory processes are ubiquitous in the brain and couple remote neuronal populations. Theta and gamma rhythms are coupled, and provide a temporal frame of reference for faster computations.

The DMN and the dorsal attention system are important for goal-directed cognition, but spontaneous fluctuations in the DMN and the dorsal attention system continue during active cognition. This tonicity presumably primes structures to infer exogenous inputs and supports a background level of predictive coding.

The give-and-take between the default system and task-positive systems appears to be vital for active cognition and conscious awareness. The default mode network is connected to the dorsal attention system, the salience system, and the hippocampal formation.

Functional connectivity in the dorsal motor network (DMN) and the dorsal attention system provides an index of cognitive aptitude but not necessarily active cognition. Ineffective deactivation of the DMN has been associated with cognitive error, negative symptoms in schizophrenia and depression.

Summary and synthesis

The secondary process, entailed by ego-functions, is associated with the suppressive effect of the DMN on its subcortical nodes and anti-correlated networks, while the primary process is manifest in non-ordinary states of consciousness.

The phenomenology of primary process thinking

In this section we describe the phenomenology of non-ordinary states of consciousness that have been associated with primary process thinking. The id and the ego are represented by the terms ‘the it’ and ‘the unconscious’, respectively.

The term ‘the id’ was introduced relatively late by Freud as a new name for ‘the unconscious’ in its systematic sense. It was useful in that it resolved ambiguities relating to the descriptive meaning of ‘unconscious’.

Primary process thinking can be measured psychophysically, for example, by observing impaired temporal perception in hallucinogenic drug states and acute psychosis. Four other qualities of primary process thinking can also be assessed empirically, including timelessness and an increase in temporal coherence.

Fear is the most frequently occurring dream emotion, and can be experienced in the aura of temporal lobe epilepsy, early psychosis, the hallucinogenic drug state, and dreaming.

The hallucinogenic drug state is characterized by distorted room and furniture, de já vu, recollective or reliving phenomena, disturbance to the sense-of-self, and relaxation of the self boundaries.

Other characteristics of primary process thinking include fear of losing control of ones mind, euphoria, grandiosity, paranoia and suspiciousness, thought-disturbances, bizarre thought-content and an increased interest in mystical, magical or animistic notions. All these states have been compared with each other previously, and all have been described as states conducive to the emergence of primary process thinking. In the remainder of this section we will review evidence that these states also possess a related neurophysiology.

Neurophysiology of the primary process

Theta activity spreading from the medial temporal lobes to the visual association cortices is consistent with Freud’s speculations about the processes underlying dreaming and related states, and increased theta power has been recorded over the medial temporal lobes during recollection using magnetoencephalography.

In the 1950s and early 1960s, activity was recorded in the septum, amygdala and hippocampus in patients experiencing acute psychotic episodes. This activity was most pronounced when the psychosis was most florid and was absent when the symptoms remitted.

Studies have shown that the medial temporal lobes of subjects administered hallucinogenic drugs show spiking and bursts of high-amplitude activity similar to that recorded in acutely psychotic patients. These studies have also shown that a specific mode of cognition rests on brain states that possess a characteristic neurophysiology.

Medial temporal lobe activities were observed to be influenced by psychiatric interview.

Theta range activity is often seen in the temporal lobe aura, acute psychosis, the hallucinogenic drug state and REM sleep, although bursts of high-amplitude fast activity are also seen. Hippocampal theta in animals is associated with locomotion, orienting and REM sleep, and also long-term potentiation. It also facilitates the retrieval of past experiences, and is likely to relate to high-amplitude bursts seen in the septum and medial temporal lobes during non-ordinary states of consciousness. In the non-ordinary states, activity recorded from the scalp and in the cortex is generally low-amplitude, high-frequency and desynchronous, and is highly characteristic of REM sleep and other cortical ‘up’ states such as those induced by serotoninergic hallucinogens.

Based on empirical findings, it has been proposed that bursts of limbic theta, recorded in the cortex as increased gamma, can index the positive symptoms of various neurological and psychiatric disorders.

Recent intracranial EEG work in humans using subdural electrodes showed that theta phase-modulation of high-frequency gamma power was evident at rest but also during behavioural tasks. Theta-gamma coupling was highest at the trough of the theta phase.

Summary and synthesis

High-amplitude low-frequency discharges in limbic and paralimbic regions index the free-energy of the Helmholtzian scheme and mediate the primary process of the Freudian scheme. In non-ordinary states, this function may be perturbed by drugs that act at modulatory post-synaptic receptors.

Neuroimaging measures of functional and effective connectivity could be employed to assess whether limbic discharges are capable of traversing systems in REM sleep and hallucinogenic drug states, and whether they are suppressed by higher-level regions of the DMN in normal waking cognition but not in non-ordinary states.

Discussion

In this article we have explored how intrinsic networks self-organize into hierarchical frameworks, and how spontaneous fluctuations in neuronal activity in cortical nodes of the DMN function to suppress anarchic activity in limbic and paralimbic systems.

Different readers will find merit in different aspects of this synthesis, but the remarkable overlap between Freud’s theories and modern neurobiology may engage clinicians and academics who are more familiar with Freud’s work and inform psychoanalytic thinking.

Freud’s writings contain many useful heuristics for exploring global brain function, especially in non-ordinary states of consciousness. The Freudian model adds a framework for an integrated understanding of psychopathological phenomena, and may dissolve naturally once the full-character of non-ordinary states and cognition is understood.

The synthesis attempted in this article is intended to facilitate a more comprehensive understanding of psychological and neurobiological phenomena. It may also provide new insights into the pathogenesis of schizophrenia, given that related symptoms are prevalent in the prodromal phase.

All we know about libido relates to the ego, which stores up the whole available quota of libido, and then invests the ideas of objects with libido.

The DMN is displaced from the dorsal attention system during goal-directed cognition.

Freud’s notion of a finite ‘reservoir’ of energy and the reciprocal patterns of activation between the DMN and subordinate networks fit comfortably with hierarchical minimization of free-energy. This entails recurrent message-passing between hierarchical brain systems that try to suppress the free-energy at all levels.

Recent work has shown that there is reduced engagement with the external world in schizophrenia, which correlates positively with connectivity in the DMN.

The brain’s hierarchical organization is use-dependent and may be jeopardized if the individual withdraws from the external world. If the ego does not develop an adult ego, the patient may develop delusions as a compromise strategy for containing the increase in free-energy.

Freud recognized that a retreat from the external world is characteristic of depression, and focused on a loss of object-love.

A process of melancholia is reconstructed as an object-choice, an attachment of the libido to a particular person, which was shattered owing to a real slight or disappointment coming from this loved person. The libido was withdrawn into the ego, which could now be judged by a special agency.

Recent work has shown that depression is associated with a reduced task-induced suppression of DMN activity, and with reduced blood flow and activation in the dorsolateral prefrontal cortex and limbic and medial prefrontal regions.

Conclusion

This article reviewed evidence that the DMN and its anti-correlated networks are consistent with the ego, and described how the DMN might be used to understand clinically relevant phenomena.

This article does not address the efficacy of psychoanalysis as a treatment, but rather the validity of Freudian constructs in relation to global phenomena and related theories that have recently emerged in systems neuroscience.

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