Excerpt from: Schleip et al. (eds.) Fascia - the tensional network of the human body.

Elsevier, Edinburgh 2012

lnteroception
A new c orrelate for intricate connections b etween fascial receptors, e mot ion, and self reco gnition

2.3
What is interoception?
Previous concepts of interoception often focused on visceral sensations only . Current concepts describe interoception as a sense of the physiological condition of the body, which includes a much wider range of physiological sensations, including, for example, muscular effort, tickling, or vasomotor sensations (see Box 2.3.1). These sensations are triggered by stimulation of unmyelinated sensory nerve endings (free nerve endings) that project to the insular cortex rather than to the primary somatosensory cortex which is usually considered as the main target of proprioceptive sensations (Berlucchi & Aglioti 20 I 0). Feelings from these sensations not only have a sensory, but also an affective, motivational aspect and are always related to the homeostatic needs of the body. They are associated with behavioral motivations that are essential for the maintenance of physiological body integrity.

Robert Schleip

Heike Jager

Introduction
While the sense of proprioception is fairly well known to therapists working with fascia, interoception and its inclusion in fascial therapies may be a "new concept" for many. The concept is not so new: in the nineteenth century it was called coenesthesia: the neurological model of a mostly unconscious sense of the normal functioning of the body and its organs. Early German physiologists called it Gemeingefuehl or "common sensations" and differentiated them from the five senses of Sherrington's early writings. Recently, however, the same concept has been intensely revived under the term interoception, and novel insights regarding the anatomical, physiological, and neurological details of this sensory system have led to an almost explosive increase of scientific attention and exploration . Disorders such as anxiety, depression, or irritable bowel syndrome have subsequently been described as interoceptive disorders. Most notably, it has been proposed that the neural pathways associated with interoception may be considered as a potential correlate for consciousness (Craig 2009). The sensory receptors for interoception are free nerve endings, most of which are located in fascial tissues throughout the human body. It is helpful to understand that proprioception and interoception are organized differently in the human brain and that very different afferent pathways are involved in them.

Sensual touch
A recent and surprising addition to the above list of interoceptive sensations is the sense of sensual or pleasant touch. This discovery was triggered by examinations of a unique patient lacking myelinated afferents in whom slow stroking of the skin with a soft brush triggered a faint and obscure sensation of pleasant touch (and general well-being), although

2012. Elsevier Ltd .

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Box 2.3.1 Interoceptive sensations

Warmth, coolness Muscular activity Pain, tickle, itch Hunger, thirst Air hunger Sexual arousal Wine tasting (in sommeliers) Heartbeat Vasomotor activity Distension of bladder Distension of stomach, rectum or esophagus Sensual touch. Afferent pathways associated with these sensations follow the lamina I spinothalamocortical tract towards the insular cortex.

the patient was unable to recognize any stroking direction. Functional magnetic imaging showed that this vague sensation was accompanied by a clear activation of the insular cortex, while no activation was seen in the primary somatosensory cortex. (Olausson et al. 201 0) . Based on the innervation of primate skin and on subs equent studies with other patients it was concluded that the affected sensory receptors are unmyelinated C-fiber afferents with <1 low mechanical threshold, and that these endings are themselves connected with neural interoceptive pathv,rays. Those afferents have a slow conduction velocity (0.5-1.0 s delay from stimulus to arrival in the brain). Since these receptor types have never been found in the palm of the hand despite numerous microneurographic re cordings, it is assumed that they are present in hairy skin only and are absent in glabrous skin . It is concluded that human skin contains particular touch receptors which form a system for social touch that may underlie emotional, hormonal (for example oxytocin), and affiliative responses to caress-like, skin-to-skin contact between individuals (Fig. 2.3.1). The profound importance of such a system for human health and well-being has long been indicated (Montague 1971), at least since the classical study of Harlow (1958) with baby rhesus monkeys that express affection for a surrogate mother in response to tactile comfort.

Fig. 2.3.1 The discovery of interoceptive receptors in human skin . Besides proprioceptive nerve endings, human skin contains Interoceptive C-fiber endings which trigger a general sense of well-being . The connections of these slowly conducting receptors do not follow the usual pathway of the pyramidal tract towards the proprioceptive areas in the brain. They rather project to the insular cortex, a key player in the regulation of interoception. This was recently discovered through experiments with patients lacking myelinated afferents. Whenever their skin was gently stroked. they responded with an increased sense of general well-being, although they were unable to detect the direction of stroking. Subsequent brain imaging studies revealed that the touch activated their insular cortex, while no activation was seen in proprioceptive brain areas. It is concluded that human sk1n contains special touch receptors, with a slow conduction velocity, which are part of a neurobiological system for social touch. i&')iStockphoto .com/Neustockimages.

A new phylogenetic development

The afferent neurons related to interoception terminate in lamina I, the most superficial layer of the dorsal horn of the spinal cord. This lamina projects strongly to the sympathetic cell columns of the thoracolumbar spinal cord, where the sympathetic preganglionic cells of the autonomic nervous system originate. From there they project to the main homeostatic integration sites in the brainstem. The latter include brainstem regions - such as the parabrachial nucleus- which are densely interconnected with the amygdala and hypothalamus. In addition, they proj ect to the insular cortex. Interestingly, this particular '' lamina I spinothalamocortical pathway" is a comparatively recent phylogenetic acquisition of primates . It evolved from the afferent portion of the evolutionary ancient system

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CHAPTER 2.3

that maintains the homeostatic integrity of the body . In mammals, the activity of lamina I neurons is integrated in the parabrachial nucleus; it is only from there that they are further projected to the insular cortex via the ventromedial thalamic nucleus (Craig 2009). In primates, however, there are direct projections from lamina I to thalamic regions from which they are further conveyed to the insular cortex (Fig. 2 .3 .2). ln other words, primates possess a more direct route between the afferent region for interoceptive sensations in the spinal cord (lamina I) and their msular cortex . No comparable difference in terms of neuronal architecture between primates and other mammals has been observed regarding their processing of proprioception. The insular cortex itself is organized in a hierarchical manner: primary sensory inputs related to interoceptive sensations project to the posterior insula. They are then progressively elaborated and integrated across modalities in the middle and anterior insula (Devue et al. 2007) . Finally, the highest

Insula

Thalamus

integrative level is expressed in the anterior insula which has intimate connections with the anterior cingulate cortex. Together they form an emotional network in which the limbic insular component is involved in sensory reception and conscious feelings, and the cingulate cortex serves as the motivational and motor component for the behavioral expression of the feelings. vVhen observing the emotional behavior of nonprimate animals, our tendency towards anthropomorphic inferences suggests that they experience bodily feelings in the same way as we do. However, their different interoceptive pathways indicate they don 't, because the phylogenetically new pathway that conveys interoceptive sensations to the thalamocortical levels in primates is either rudimentary or absent in nonprimate animals (Craig 2003). The anterior insula-cingulate network is also credited with the specific function of self recognition (Devue et al. 2007). Craig (2009) provided impressive evidence that the anterior insular cortex is a peculiarly human brain structure that is crucial for integrating all subjective feelings related to the body, and especially to its homeostatic conditions, into emotional experiences and conscious awareness of the environment and the self. He suggests that the human insular cortex and its peculiar spinothalamic afferent pathways set our species apart from other mammals by supporting consciousness of the body and the self. This view is congruent with the somatic marker hypothesis of Damasio (1994), which proposes that humans use nonconscious somatic sensations, such as "gut feelings", to guide their decision making, particularly when facing complex and conflicting choices. Similar to Craig's concept of the uniqueness of human interoception, this model sees the human insular cortex- together with its newly acquired direct spinothalamic afferent pathway -as key players for the integration of body perceptions and mental processes.

Fig. 2.3.2 A novel short-cut route for interoception in primates. In mammals , the main pathway of interoception starts with free nerve endings, which project to the lamina I of the spinal cord. From here they project to the prebrachial nucleus in the brainstem, and it is only from there that they are further projected to the insular cortex via the thalamus. In primates, however, there are additionally direct projections from lamina I to the insula via the thalamus. Primates therefore possess - as a novel phylogenetic acquisition - a more direct route between the afferent region tor interoceptive sensations in the spinal cord and the insular cortex (black arrow).

lnteroception and somatoemotional disorders

The described (re)discovery of the importance of interoception in human self regulation - and of the unique neural architecture that regulates the processing of these internal body sensations in humans triggered a multitude of studies examining the correlations between interoception and particular
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aspects of human health. Apparently, many complex disorders with a somatoemotiona] component are associated with clear differences in interoception . While this is currently a new and exciting field of research in psychobiological medicine, many of the studies so far published reveal an association of such pathologies with interoceptive processing. However, the precise system dynamics of these associations (including the differentiation between primary causative and secondary effects) still need to be elucidated for most of the interoceptive disorders. The following disorders are examples of such complex interactions. Anxiety, as well as depression, has been shown to go along with significant alterations in interoceptive processing. They are connected with increased but noisy interoceptive input, the processing of which is amplified by self-referential belief states via an enhanced top-down modulation in response to the poorly predictable interoceptive states (Paulus & Stein 2010). Both of these somatoemotional disorders seem not to be disorders of the afferent interoceptive signaling, but can be understood as altered interoceptive states as a consequence of noisy amplified self-referential belief states concerning the interoceptive sensations. Similarly, brain imaging studies of patients vvith irritable bowel syndrome revealed a disrupted modulation of insular cortex responses to visceral stimuli (such as in response to experimentally induced painful rectal distension as well as to the subsequent relaxation). It is suspected, that these dysfunctional regulations may provide the neural basis for altered visceral interoception by stress and negative emotions in these patients (Eisenbruch et al. 2010). Drug addictions, as well as other addictions, have also been proposed to be interoceptive disorders. Apparently, the primary goal of these disorders is that the addicted individual aims to obtain the effects of the drug use ritual upon their internal body perception. The representations of the achievement of this goal in interoceptive terms by the insula contribute to how addicted individuals feel, remember, and decide about performing the related rituals. Similar interoceptionrelated insular dynamics have been suggested for other addictions and cravings, such as excessive sex, gambling, smoking, or eating (Naqvi & Bechara 201 0) . In essential hypertension an increased interoceptive awareness has been observed, even in the early stages of this disorder, and its contribution to the prospective development of this common cardiovascular syndrome has been discussed (Koroboki et al. 201 0).
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Finally, aging and post-traumatic stress disorders have been shown to be associated with a significant decline in interoceptive awareness. Mindfulnessbased therapies, focusing on subtle somatic sensations are therefore suggested as helpful therapeutic approaches (van der Kolk 2006).

Fascia as an interoceptive organ

In musculoskeletal tissues only a minority of the sensory nerve endings are myelinated mechanoreceptors concerned with proprioception, such as muscle spindles, Golgi receptors, Paccini corpuscles, or Ruffini endings. The vast majority - or 80;(> of afferent nerves - terminate in free nerve endings (Schleip 2003) . Termed "interstitial muscle receptors", they are located in fascial tissues such as the endomysium or perimysium and are connected with either unmyelinated afferent neurons (then called type IV or C-fibers) or myelinated axons (type III or A'6 fibers). Indeed, 90% of these free nerve endings belong to the first group, to the slowly conducting C-fiber neurons (Mitchell & Schmidt 1977). Functional magnetic imaging studies by Olausson et al. (2008) revealed that stimulation of these C-fiber neurons results in activation of the insular cortex (which indicates a clear interoceptive role of these receptors) and not of the primary somatosensory cortex which is usually activated by proprioceptive input. A surprising conclusion from this is that the number of interoceptive receptors in muscular tissues by far outnumbers the amount of proprioceptive endings . In numerical terms, one could estimate that for every proprioceptive nerve ending in these tissues there are more than seven endings that could be classified as interoceptive receptors. While some of these free nerve endings are thermoreceptors, chemoreceptors, or have multimodal functions, the majority of them do in fact function as mechanoreceptors, which means they are responsive to mechanical tension, pressure, or shear deformation. While some of these receptors are high threshold receptors, it has been shown that a significant portion (approximately 40%) can be classified as low threshold receptors, which are responsive to light touch, even to touch as light as "with a painter's brush" (Mitchell & Schmidt 1977). Most likely they are therefore also responsive to the tissue manipulation of myofascial therapists .

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CHAPTER 2.3

Manual therapy and interoception

When treating muscular tissues myofascial therapists are usually concerned with direct biomechanical effects on non-neural tissues or with the stimulation of specific proprioceptive nerve endings, such as muscle spindles, Golgi receptors, etc. However, the above considerations suggest that it IS advisable that manual therapists target the interoceptive receptors and their related upstream effects to a much larger degree than is usually taught or practiced. Some of the interoceptive nerve endings in muscle tissues have been classified as ergoreceptors; they inform the insula about the work load of local muscle portions. Their mechanical stimulation has been shown to lead to changes in sympathetic output, which increases the local blood flow. Stimulation of other interoceptive nerve endings has been shown to result in an increased matrix hydration, via an augmentation of plasma extravasation, i.e., the extrusion of plasma from tiny blood vessels into the interstitial matrix (Schleip 2003) . It could therefore be extremely useful to pay attention to the autonomic responses at each moment - and to the limbic-emotional (or insular) response of the client, while monitoring the touch direction (plus its speed and magnitude) in such a manner that a profound change in local tissue hydration as well as other autonomic effects can be achieved. lt would also be advisable to invite a perceptual refinement - and some verbal feedback of the client regarding their interoceptive perceptions. While proprioceptive sensations may be in the foreground during the actual stroke application, those finer interoceptive sensations are usually easier to perceive in periods of at least several seconds of rest between different manipulative strokes . Subjective sensations of warmth, lightness/ heaviness, spaciousness, density/ fluidity, nausea, streaming, pulsation, spontaneous affection, or a general sense of well-being may be such interoceptive sensations that can be triggered by myofascial tissue manipulation. From the therapist's perspective, subtle changes in the client- such as an increased local tissue hydration, changes in temperature, in skin color, in breathing, micromovements of the limbs, pupil dilation, and facial expression- can serve as valuable signals for physiological effects related to interoceptive processes . Therapists who apply mechanical stimulation to visceral tissues, such as visceral osteopaths, should

also profit from a larger recognition of interoception and related physiological as well as psychoemotional effects. Recent discoveries concerning the richness of the enteric nervous system have taught us that our "belly brain " contains more than 100 million neurons (Gershon 1999) . Most of these are located either in the connective tissue zone between the inner and outer layers of the muscularis externa (Auerbach's plexus) or in the dense connective tissue layer of the submucosa (Meissner 's plexus). Many of these visceral nerve endings are directly concerned with interoception and are connected via the "lamina 1-spinothalamocortical pathway" with the cortical insula, as described above . Considering that several complex disorders such as irritable bowel syndrome are associated with a disrupted modulation of insular responses to visceral stimuli, it is conceivable that a slow and careful application of manual forces to visceral tissues- if accompanied by a sense of safety and mindfulness of the client - could be a useful, if not ideal, approach for enhancing a healthy interoceptive self regulation. Myofascial as well as visceral therapists should also not be surprised when encountering psychoemotional responses which may include changes in internal body perception, in self awareness, or affiliative emotions. These may be triggered by their stimulation of interoceptive free nerve endings in the skin, in visceral connective tissues as well as in muscular tissues.

Movement therapies and interoception

In competitive sports, the attention is often focused on external goal achievements. Frequently, it is also focused on the task of overriding internal sensations of discomfort, tiredness, etc. In contrast, complementary medicine associated practices - like Yoga, Tai Chi, Chi Gong, Feldenkrais, Pilates, Body Mind Centering, or Continuum Movement - usually encourage a perceptual emphasis on finer sensations in one's own body. However, depending on the focus of the individual teacher or respective school, the internal perception is sometimes directed almost entirely towards proprioceptive refinement. For example, a student of such training approaches may learn to feel minute movements of individual vertebrae or to control their lumbar lordosis within a multitude of loading situations. Nevertheless, they may remain an
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"interoceptive moron", who may, for example, be unable to differentiate whether their visceral sensations at a given moment are signs of an empty stomach, of stage fright-induced ''butterflies", of empathy-driven "gut feelings" about another person's dilemma, or may simply be an acute gastritis. Jn contrast, some teachers of these practices also include a skilled fine-tuning of the student's perception for interoceptive sensations. This may include emphasizing sensations such as a subtle tingling under the skin, sensation of a general or localized warming, a subjective sense of internal spaciousness, a feeling of aliveness, an inner silence, an emotional ''homecoming", or a meditation-like change in general self awareness. For example, gravity-oriented changes in body positions- such as some upside-down postures in yoga practices - could easily trigger new and interesting (and hopefully unthreatening) sensations in visceral

ligaments, which can foster interoceptive refinement. Given the recent research indications for a close correlation of many psychoemotional disorders such as irritable bowel syndrome, anxiety, or posttraumatic stress disorder - with a disrupted interoception, it is conceivable that some of these movement practices may have a strong therapeutic potential for these disorders. Typically, these therapeutic practices foster an attitude of inner mindfulness, of refining "internal listening skills", and they frequently alternate brief periods of active motor attention with subsequent periods of rest where the students pay attention to small interoceptive sensations vvithin their body. Not surprisingly, some studies already indicate a positive health-enhancing effect of such "mindfulness based therapies" for a large number of common clinical conditions (Astin et al. 2003).

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