neurocoverThis is the second post looking at Karl Friston’s review (“The Fantastic Organ” Brain 2013:136; 1328-1332) of Kandel’s The Age of Insight: the Quest to Understand the Unconscious in Art, Mind, and Brain, from Vienna 1900 to the Present. Kandel looks at how we make inferences about other people, ourselves and our emotional states. He combines the mirror neuron system with reflections in a mirror. Friston suggests that this captures the essence of ‘perspective taking’, which is unpacked in terms of second order representations (representations of representations) as they relate to theory of mind and how artists use reflections. Friston states:

It is self evident that if our brains entail generative models of our world, then much of the brain must be devoted to modelling entities that populate our world; namely, other people. In other words, we spend much of our time generating hypotheses and predictions about the behavior of people—including ourselves. As noted by Kandel ‘the brain also needs a model of itself’ (p. 406).

According to Friston this places the mirror neuron system center stage in generating predictions about how we will behave. In discussing this, Friston brings up three terms that were new to me. I will try to explain them as an aside.

Proprioception is the sense of the relative position of neighboring parts of the body and strength of effort being employed in movement. The proprioceptive sense is believed to be composed of information from sensory neurons located in the inner ear (motion and orientation) and in the stretch receptors located in the muscles and the joint-supporting ligaments (stance). Proprioception is sometimes said to combine the kinaesthetic (extremities) system and the vestibular (inner ear) system. It is distinguished from exteroception, by which one perceives the outside world through specific receptors for pressure, light, temperature, sound, and other sensory experiences, and interoception, by which one perceives pain, hunger, etc., and the movement of internal organs.


To appreciate the bilateral nature of predictions provided by the mirror neuron system, Friston suggests that we have to take unconscious inference to the next level and consider it in an embodied context. Put simply, one can regard perception as the suppression of outside the body prediction errors by selecting predictions that are best able to explain sensations. However, exactly the same argument can be applied to action that minimizes inside the body prediction errors via the classical reflex arcs. In other words, we can reduce prediction errors in one of two ways: we can either change predictions so that they match (exteroceptive) sensory samples, or we can change the samples through action, to make them match (proprioceptive) predictions. This is active inference. So what has this got to do with mirror neurons? If mirror neurons provide top-down predictions of both the proprioceptive and exteroceptive consequences of moving—and thereby cause movements through motor reflexes, then they provide a ready-made set of hypotheses for inferring the motor intentions of other people. This is because the exteroceptive (e.g. visual) consequences of movements are the same and all we have to do is to suppress the proprioceptive predictions. This provides a  perspective on why mirror neurons respond both to self-made acts and during action observation.

‘just as the visual brain constructs models of reality from figural primitives, so our social brain is innately wired to function as a psychologist, forming models of other people’s motivations, desires and thoughts.’ (p. 406)

However, Friston suggests that there is an important twist here. To harness the mirror neuron system during action observation, we have to suppress proprioceptive prediction errors that would otherwise elicit movements and cause us to mimic (mirror) the subject of our observation. This suppression rests on (mathematically speaking) reducing the precision of—or confidence in—proprioceptive prediction errors. This speaks to fundamental aspect of inference in the brain; namely the encoding of precision or confidence through neuromodulation. In other words, not only do we have to infer the content of our sensory apparatus but also the context, in terms of the precision or certainty about the content. This represents a subtle but always present problem that the brain has to solve—and the solution rests on modulating the gain or post-synaptic sensitivity of neuronal populations encoding prediction error.

Friston goes beyond Kandel’s book when he introduces neuromodulation as the neuronal basis of precision (the encoding or representation of uncertainty). This ties inference in the brain to synaptic processes that may be compromised in syndromes like schizophrenia, Parkinson’s disease, autism, hysterical disorders, and so on. The basic idea is that many disorders of active inference can be understood as a failure of neuromodulation.  Friston suggests that the biggest challenge to formal descriptions of the brain as an inference machine is how one can accommodate emotions, self-awareness and disorders thereof. Prediction errors are formed by comparing primary input from stretch receptors with descending proprioceptive predictions to alpha motor neurons in the spinal-cord (and cranial nerve nuclei). This view replaces descending motor commands with motor predictions that are fulfilled by peripheral reflexes. The predictions themselves are elaborated on the basis of deep hierarchical inference about states of the world, including the trajectories of our own bodies. Friston believes that exactly the same mechanism can be applied to interoceptive signals. This means that the internal milieu is controlled by autonomic reflexes that transcribe descending interoceptive predictions into a physiological homoeostasis. As with the mirror neuron system (and sensorimotor representations in general), these interoceptive predictions are just one—among many—of multimodal predictions that come from high-level hypotheses about our embodied state.

Friston says that the best explanation for the myriad of sensory inputs I am experiencing is my situated state of mind. A situated state that comprises an internally consistent hierarchical model of the world, with multiple levels of description. Crucially, these hierarchal representations also predict my interoceptive state; including sympathetic and parasympathetic outflow—literally, my gut feelings. In this view, interoceptive information does not cause our self-awareness, or vice versa. There is a circular causality in which neuronal representations cause changes in autonomic status by enslaving autonomic reflexes. At the same time, interoceptive signals entrain hierarchical representations so that they provide the best prediction. Emotional valence is therefore a necessary aspect of any representation in the brain that includes interoceptive predictions. This means that—in terms of the brain’s computational anatomy—the influence of gut feelings (interoceptive signals) is inherently contextualized by concomitant exteroceptive and proprioceptive input. As Kandel observes:

‘As with visual perception, where we have learned that the brain is not a camera but a Homeric storyteller, so with emotion: the brain actively interprets the world using top-down inferences that depend upon context. As James pointed out, feelings do not exist until the brain interprets the cause of the body’s physiological signals and assembles an appropriate, creative response that is consistent with our expectations and the immediate context.’ (p. 351)

This is interesting stuff even though my understanding is weak.

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