Pain in PDOC

PDOC stands for Prolonged Disorder of Consciousness; the term covers two previously defined states: vegetative and minimally conscious. This post considers the question, “Does a person in a prolonged disorder of consciousness experience pain?” This question covers both pain caused by care or treatment and pain arising secondary to consequences of nerve damage, such as from prolonged immobility or spasticity. I am frequently asked by the families of and the clinicians caring for patients in a prolonged disorder of consciousness whether the person can feel pain. In this post, I will develop my thoughts and arguments. I will stress from the outset that no one can know definitively, not least because no one can know definitively what any other person experiences, even when conscious. One well-known variation on the question is to ask yourself the question posed by Thomas Nagel in 1974, “What is it like to be a bat?”. I will explore the conceptual and neuroanatomical differences between consciousness, awareness, and experience to answer the question.

Table of Contents

Introduction

My interest in this was crystallised by a legal case where the question of how much pain is experienced was a significant concern. The case concerned a two-year-old child, but the considerations are no different. This post will work through an argument step by step. The first step is to consider consciousness – what is it? The Oxford English Dictionary describes consciousness as “the state of being aware of and responsive to one’s surroundings“. This immediately raises two questions:

  • Does a lack of consciousness imply a lack of responsiveness?
  • Are consciousness and awareness synonymous?

Whenever consciousness, awareness, and experience are discussed, we start considering deep philosophical questions. They will arise in this post, but I will refrain from analysis in the depth associated with philosophy.

PDOC: consciousness and responsiveness

Being unconscious is not the same as being unresponsive. The importance of this crucial distinction was brought home to me by the mother of a patient who was, in our view, in a prolonged disorder of consciousness. When discussing our clinical findings and giving her our conclusion that her son was completely unaware, she said, “But he can’t be because he moves when I touch him, and he opens his eyes when I talk.” We agreed that both her observations were accurate.

I suddenly realised that we had been talking at cross purposes. She thought that being unaware meant being completely unresponsive. We thought being unaware meant (or was demonstrated by) a lack of behaviours that required the person to extract abstract meanings from stimuli or to need the person to formulate abstract goals and show actions that carried meaning.

An unconscious person responds to stimuli. Indeed, the Glasgow Coma Scale measures the depth of a coma by measuring how responsive someone is. Patients with the lowest six levels of coma (scores 3/15 to 8/15) are considered unconscious. The distinction arises from differences in their response to pain and other stimuli. Moreover, unconscious people demonstrate many reflex responses such as constriction of pupils to bright light, startle to sudden loud noise, and tendon jerk reflexes.

Therefore, it is essential to understand that responses to stimuli do not necessarily imply conscious awareness. As discussed later, the complexity of a response or behaviour guides the judgement of a person’s awareness.

Reflex and automatic responses.

It is too easy to say about a response: “That’s just a reflex response.” While most people understand the knee-jerk tendon reflex and the reflex of pupillary constriction to bright light, they quite rightly become suspicious if more complex responses are described as a reflex. When I accidentally walk into someone, I say ‘Sorry’ and, if asked, I might explain that as a reflex. Simple social responses are often made without conscious thought; I have apologised to more than one parking meter in London! [Historical note for younger readers: a parking meter was a column about one meter tall with a meter that accepted money and licenced your car’s stay in the parking space for the time bought.]

There are simple reflex responses that have one or two synapses. In plain English, the signal goes from an input to output directly or through one intermediate nerve cell. Tendon jerks are the most straightforward; the withdrawal of a limb in response to pain is another. These can readily be termed reflexes, occurring without conscious thought or awareness. Nevertheless, even these reflexes can be suppressed or enhanced consciously to a certain extent.

Many other responses are generally not within direct conscious control but involve more nerve cells and complex pathways than the simple reflex. Examples include grimacing (drawing back of the lips) and increased pulse rate in response to pain, sudden startle movements of much on the body in response to a sudden loud noise, and looking at an object entering the visual field fast, such as a ball coming towards one.

These behaviours are better classified as automatic to acknowledge they are more complex than simple reflexes. The complexity varies. Some are complex learned behaviours that have become unconsciously undertaken, whereas others remain simple protective behaviours.

There are many automatic responses of varying degrees of complexity, up to and including using standard phrases such as “OK, thank you” in response to “How are you?”. Most are less complex than that, and many can be consciously suppressed. Indeed, some automatic responses may indicate reduced conscious control over behaviour. One example is the disinhibited behaviour in people who have taken too much alcohol.

Therefore, it is crucial to recognise that some quite complex responses to stimuli are automatic in that they do not require or depend upon any complex processing of information. They are behaviours that are learned but become so built-in that they occur without any conscious thought; consciousness may control them, but it does not cause them.

Consciousness and experience

Whole books are written about consciousness from many different perspectives. These brief few paragraphs will consider it from a neurological and practical perspective, sufficient to justify an answer to the question, does someone with a prolonged disorder of consciousness experience pain?

Consciousness is a record of what we have done, and the perception that we consciously control our behaviour and make decisions is an illusion. This is widely felt to be the case. Two accessible papers will explain the evidence and how consciousness arises in detail for anyone interested. (here and here) In the meantime, you can consider consciousness as a delayed film, showing ‘you’ what ‘you’ experienced or decided a few milliseconds ago. This does not absolve us from responsibility for our actions!

The underlying neurophysiology and neuroanatomy are subject to debate, and there are many theories, including one involving quantum theory! (here) For an overview of ideas, see here and here.

There is no centre for awareness that, if damaged, inevitably leads to loss of consciousness.

Consciousness arises, in some way, from the entire brain. People with prolonged disorders of consciousness usually have damage that:

  1. includes both cerebral hemispheres, the thalamic nuclei, and other basal ganglia nuclei, and
  2. is diffuse and widespread.

Damage like this will inevitably disrupt and often prevent the function of widespread cerebral neural networks. Most theories about consciousness consider it arises from the integrative role of neural networks within the brain; two illustrative papers can be found here and here. Thus, these theories predict that patients with widespread damage affecting all parts of both cerebral hemispheres would be left with a prolonged disorder of consciousness.

In summary, consciousness depends on and arises from large-scale networks within the brain traversing almost all areas, from the basal ganglia to both cerebral hemispheres. A prolonged loss of consciousness occurs after damage to the nerve cells and tracts that form these networks, and this damage must be widespread involving the basal ganglia and hemispheres.

Consciousness – and awareness.

The Oxford English Dictionary describes awareness as “knowledge or perception of a situation or fact”. In the context of this discussion, stating that a patient is or is not aware will be focused on perception. However, it is not quite what is meant. Self-awareness is described as “conscious knowledge of one’s own character and feelings”, which is more focused on insight into one’s state than it is focused on being aware in contrast to being unaware.

Consciousness and awareness are used almost interchangeably. However, consciousness also encompasses a person’s level of arousal, whether they are aware. The difference was explained concisely by Ferris Jabr, “Consciousness is awareness of one’s body and one’s environment; self-awareness is recognition of that consciousness—not only understanding that one exists but further understanding that one is aware of one’s existence. Another way of thinking about it: To be conscious is to think; to be self-aware is to realise that you are a thinking being and to think about your thoughts.”

Minji Lee and colleagues also discuss arousal, consciousness, and awareness as interdependent and overlapping concepts that are separable when measured appropriately.

For the remainder of this post, I will use being conscious as a generic term that includes being awake and analysing stimuli sufficiently to perceive their meaning and plan a complex and meaningful response. I will use awareness, being aware, to refer to a higher, reflective level of function where the person can appreciate and communicate that they have a subjective experience of the perception.

Clinical assessment of awareness

The central question asked about someone who is, in everyday language, unconscious is, “Are they aware of anything?”. This can be refined into three questions:

  1. Is she (or he) aware of what is going on around her?
  2. Is she aware of her bodily sensations and what is happening to her?
  3. Is she aware of her situation?”

These questions require the patient to recognise that sensations imply something more, as something requiring analysis, which ends up with the person developing an internal model of their situation and appreciating that they have done so. This is a very complex activity. It is the function of the many networks within the brain that, if different from those underlying consciousness, will be very closely related.

The question is perhaps best phrased as “Does the patient have ‘self-awareness’, the ability to analyse sensory stimuli and interpret them as experiences with meaning?

Although this is slightly off the point (about pain), it leads to a brief comment on the awareness assessment. Only a human can decide if another human is aware. No unique, single observation, test, or behaviour proves it. It is a judgement based on the observed or recorded pattern of behaviours.

I ask myself, “Do these behaviours require the person to abstract meaning from stimuli received? Do these behaviours depend upon the person having an abstract goal or appreciating that the behaviour carries a meaning? Or are there other more probable explanations? “ I acquire as many credible reports and behavioural observations as possible, including making observations myself, to judge whether only self-awareness can explain the observations. There should be reasonably frequent and consistent reports so that coincidence, automatic behaviours, and biased observations or reporting are unlikely explanations.

Thus, consciousness and awareness are closely intertwined concepts and depend upon identical or closely interwoven neural structures and mechanisms. A behavioural assessment allows a clinical judgement of the extent of self-awareness, better termed and awareness of him- or herself as a person. This judgement depends upon evidence that the person extracts conceptual meaning from stimuli through generating specific actions related to that meaning or can form an internal abstract goal leading to evidently purposeful behaviour.

Experience.

An exciting paper explores the nature of ‘subjectivity’, equivalent to a person’s ‘experience’. (here) The hypothesis is set out by the author in these words:

“In this paper, a different perspective is adopted: the modes of information processing by neuronal circuits are examined to explore to what extent a subjective and personal perspective might arise as an emergent property of the complex neural networks in the brain. This analysis reveals an intrinsic relational nature of neuronal elaboration; in particular, such relational nature appears to be inherently self-centred and furthermore, all activities in the brain (anything which is sensed/experienced) are analysed and perceived in terms of their vital, emotional and operative relevance for oneself. This suggests that a subjective dimension (self-centred relational analysis) and a personal perspective (emotional, affective, operative relevance for the self) intrinsically characterise cerebral activity and are not “added” a posteriori by some subjective observer function (consciousness) to an initially detached, objective representation of reality.

He illustrates his core ideas in Figure 5. The brain analyses a stimulus to determine

  1. whatthe stimulus represents, 
  2. wherein space, relative to the person, the impulse arises, and
  3. the emotionalassociations attached to the stimulus that
  4. affects how strongly the stimulus is memorised.

The output of this analysis is a personally relevant representation, which is then further processed by other areas within the cerebral cortex. In addition, other networks can increase or decrease the processing of different stimuli streams, giving rise to selective attention by altering the content passed on to the cortex.

The author suggests that different ‘products’ arise from the processed stimuli, which are intrinsically personalised by the initial processing, such as knowledge, personal meaning, symbolic representation, and many other higher-order phenomena.

The paper is an attempt to understand how subjective experience arises. The details are likely to need correction. The critical point made by the article is that the emergence of many of the aspects of consciousness that we take for granted – a sense of one’s own body, a feeling of being present personally in a place at a time, the memory of the past and expectation of a future, imagination etc. – all arise from and depend upon very complex processing of data in multiple networks distributed throughout most of the brain. Significant structural damage to these networks will disrupt and usually stop the processing, removing the possibility of subjective experience.

This hypothesis is strikingly similar to the idea put forward by Christof Koch, a theory I have described in another post on ‘consciousness, cause and effect’.

Pain in prolonged disorders of consciousness.

Long books are written about pain from many perspectives. These few paragraphs will focus on aspects that are germane to the question. A brief introduction to some of the essential ideas and facts can be found here.

Nociceptive pain reflexes are present in all animals, down to single-celled creatures such as amoebae. In animals with nervous systems, some pathways take information from nociceptors (organs that detect harmful stimuli) up to the central areas where responses are generated. Many of these responses are automatic: withdrawal from pain, increased heart rate, increased alertness, etc.

Thus, response to stimuli associated with tissue damage has been present from the first stages of cellular life. Unless one can attribute the experience of pain to all living animal cells, including single-celled animal organisms, the occurrence of automatic and, at times, complex responses to nociceptive (painful) stimuli cannot be taken as proof of awareness or experience.

Unsurprisingly, there is much research into, and even more debate about, the underlying neuroanatomical, neurophysiological, and chemical basis of the experience of pain. Some critical points arise.

The areas of pain that are active when pain occurs are widespread, which led to the concept of a pain matrix. However, the pain matrix is similar to the networks that analyse all sensory input. (here)

It is also widely recognised and indeed is shared experience, that psychological factors such as emotional state, expectation, fear that pain may arise and so on have a significant impact on the experience of pain. For example, pain is part of depression.  No one doubts that depression is a significant cause of pain. Yet, it does not result from nociceptive stimuli from any specific body part consequent upon tissue damage. I give more detail in my post on chronic non-malignant pain.

The experience of pain also raises philosophical problems. This is illustrated by asking, “When you hit your thumb with a hammer, where do you feel the pain in your thumb or brain?” This is an example of a potential mereological fallacy: “ascribing to a part of a creature attributes which logically can be ascribed only to the creature as a whole.” (here) In other words, you feel the pain; it is not ‘felt’ or experienced by any one part of you. It arises from you, your whole body. Without a damaged thumb, there would be no pain; without a brain, you would not perceive the pain, and without your heart, your brain would not function.

I will extract from clinical and experimental studies the main points relevant to the question about pain in people with a prolonged disorder of consciousness:

  • there is no single specific cerebral location that ‘feels’ pain, or that is always involved;
  • the experience of pain involves emotion, expectation and many other phenomena over and above tissue damage;
  • the areas of the brain usually activated by pain and involved in the experience of pain can be activated in the absence of a nociceptive input;
  • the experience of pain is associated with widespread cerebral networks not dissimilar to the networks involved in being conscious and aware.

In summary, the evidence suggests that the experience of pain is closely associated both neuro-anatomically and functionally with the same systems needed to generate and sustain consciousness and awareness of self. Consequently, it seems unlikely that damage sufficient to result in a prolonged disorder of consciousness could leave intact and functioning the mechanisms for generating the experience of pain.

Conclusion

Patients with a prolonged disorder of consciousness are very unlikely to experience pain. It is doubtful that the person has any reflective awareness of themself sufficient to think, ‘this hurts’ or ‘I am suffering pain’. My reasoning is as follows. Lack of consciousness, and hence lack of awareness of yourself as a person with a past, a present, and a future, arises from a failure of networks in the brain that process and analyse incoming stimuli (information). These networks extend through most of the brain, including both cerebral hemispheres and the basal ganglia lying underneath and within the cerebral hemispheres. The experience of pain arises from a network in the same areas.

Moreover, experience of any kind is a part of consciousness and awareness of oneself. There is no system for pain independent of the one that supports consciousness. Therefore, there is no mechanism by which some could experience pain while still unconscious. The behaviours and movements seen in unconscious people when given or having sensory input that would cause a conscious person to experience pain are automatic, not requiring and not indicative of consciousness.

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