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Pain as an Embodied Emotion
Since William James first proposed somatic responses as the
foundation of emotion in the 19th century, there has been a
vigorous debate about the role of the body in shaping emotional
experience. James’ original view was that the mind perceives a
physiological response and that the particular nature of this
peripheral response determines the emotion.(James, 1884) Based on
evidence that de-afferentation left emotional responses intact and
that physiological responses are relatively slow and non-specific,
the Canon-Bard theory proposed that brain and somatic responses to
stimuli occur simultaneously and relatively independent of each
other.(Cannon, 1927) Later cognitive theories suggested that it is
the brain’s evaluation of somatic signals that determines the
emotional experience.(Lazarus & Folkman,, 1984) Despite these
challenges and alternative theories, James’ original theory remains
influential, spawning new theories of how the peripheral responses
contribute to emotional experience(Kreibig, 2010). These include
Damassio’s Somatic Marker Hypothesis, which emphasizes the role of
somatic signals in generating emotions, particularly within the
context of decision making. The Somatic Marker Hypothesis outlines
a more active role for the brain than James’ original theory,
allowing that the brain encodes somatic states in a way that allows
emotional states to occur independent of peripheral input.(Damasio,
1991)
The nature of the interaction between brain and body that gives
rise to specific emotions continues to be a subject of intense
study. One approach to better understanding this interaction is to
study one specific emotional experience to determine how each part
of the body-brain axis contributes to what makes that emotion
unique. In this respect, pain might be particularly instructive.
The International Association for the Study of Pain has defined
pain as “an unpleasant sensory and emotional experience associated
with actual or potential tissue damage, or described in terms of
such damage”.(Merskey, Bogduk, & ., 1994) Within the context of
this discussion, it is noteworthy that pain is viewed as both a
sensory and emotional experience, but also that potential damage to
the body is at the core of the experience. The fact that the
emotional experience of pain is focused on events occurring in the
body, and that it is encoded along with sensory information such as
location and temporal characteristics suggests that information
from the body might play a particularly strong role in shaping the
emotional experience. As such, it might serve as a model for how
the body can contribute to an emotion in a way consistent with
James’ original vision.
IS PAIN SPECIFIED IN THE BODY?
Viewed within a Jamesian framework, we would expect the specific
emotional experience of pain to correspond to a specific somatic
representation. Such a representation might take the form of
receptors that are largely specialized for processing nociceptive
inputs. The existence of primary afferent nociceptive receptors has
been central to a long standing historical debate regarding whether
pain is the product of specific, labelled lines, or a pattern of
distributed inputs. The specificity account is commonly associated
with Rene Descartes, and was accompanied by Louis Lafarge’s famous
diagram (see Figure 1 below) which conveyed Descartes’ hypothesis
that that the pain system consists of a direct line from the skin
to a pain centre in the brain.(Descartes, Clerselier, LaForge,
& Schuyl, 1664) Activation of this line was viewed as necessary
and sufficient for the experience of pain, with the implication
that the pain experience corresponded to peripheral input in a 1:1
fashion. The brain is viewed largely as a relay centre for messages
from the periphery, as evidenced by Descartes’ metaphor of the
brain as a bell to be rung by tugging on a string in the
periphery.
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FIGURE 1: Lafarge’s depiction of a direct line for pain
Muller’s doctrine of specific nerve energies(Muller, 1840)
provided early theoretical support for the specificity view. Muller
posited that perceptual experiences are the product of the pathways
through which they are transmitted. The brain receives information
about the external world from sensory nerves, with the quality of
sensation determined by specific coding (which Mueller viewed as
either a product of the specific energy of individual sensory
nerves or the properties of the brain region on which they
terminate). This theory was supported within the tactile domain by
the discovery of receptors for specific tactile experiences (e.g.
Meissner’s corpuscles responding to touch, Ruffini’s corpuscles
responding to warmth and Krause end bulbs responding to cool).
Maximillion von Frey hypothesized that in addition to these
specific receptors for touch, warmth and cold, the sensation of
pain was subserved by free nerve endings.(vonFrey, n.d.) Based on
the work of Blix, Goldscheider and Donaldson, von Frey further
suggested that there was anatomical specificity for these various
tactile sensations, such that stimulation of different areas of
skin would preferentially produce percepts corresponding to the
type of receptors.(Norrsell, Finger, & Lajonchere, 1999) This
“anatomical assumption” has not been supported by subsequent
research but the “physiological assumption” of receptor specificity
remained influential and critical to subsequent research on
nociception-specific receptors.(Melzack & Wall, 2004)
An alternate, pattern-based theory was proposed by Nafe
in1929.(Nafe, 1929) Nafe suggested that it was not the specificity
of the receptor that determined the experience, but rather the
spatial and temporal pattern of discharge, which changed according
to the type of stimulation. This pattern of discharge could also be
coded across a population of afferent fibres, explaining the
variation in perceptual experience. While this theory was strongly
challenged at the level of primary afferents (see below), it has
remained highly influential, particularly at higher levels of the
neuroaxis.
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The specificity account of pain was reinvigorated by the
discovery of peripheral nerve endings selectively responsive to
stimuli in the noxious range. Sherrington’s prescient description
of “nocicipient” cutaneous end-organs specific for noxious
stimuli(Sherrington, 1903) followed on from von Frey’s theories and
was later validated by the discovery of “nociceptors”: primary
afferents responsive only to stimuli that could result in potential
injury. Some of these were specific to mechanical
stimulation(Burgess & Perl, 1967) while others were
polymodal(Bessou & Perl, 1969).
As our understanding of nociceptors has grown, the variety and
specificity of information sent to the spinal cord has become
apparent, with the structure of the nociceptor supporting the
perceptual, emotional and behavioural response to stimulation. For
example, A-delta fibres are small (1-6μm), myelinated fibres that
convey nociceptive information quickly (5-36 m/s), allowing them to
contribute to “first pain”, while C-fibres are unmyelinated fibers
whose slow (0.2-1.5 m/s) but sustained firing is responsible for a
lasting “second pain”. These fibres are, in turn, commonly
associated with different behavioural responses, with first pain
eliciting immediate withdrawal responses and second pain associated
with behaviours aimed at protecting the body and nurturing injury.
Behavioural routines are further specified by nociceptors
specifically responsive to different modalities of noxious
stimulation (e.g., hot, cold, chemical etc.).(Basbaum, Bautista,
Scherrer, & Julius, 2009; Cavanaugh et al., 2009; Julius &
Basbaum, 2001) The heterogeneity and functional specificity of
nociceptors has led many contemporary theorists to conclude that
the specificity account of pain was largely correct, at least to
the level of the spinal cord (cf. Editorial “Specificity versus
patterning theory: continuing the debate” by Allan Basbaum and
accompanying discussion by Woolf, Casey, Fields and Apkarian, Pain
Research Forum, 2011:
http://www.painresearchforum.org/forums/discussion/7347-specificity-versus-patterning-theory-continuing-debate).
This pre-spinal level of specificity suggests that the emotional
experience of pain can be largely shaped by the peripheral input
that is received. First, firing of nociceptors automatically
signals the potential for injury, therefore conferring biological
significance on the eliciting stimulus and priming threat routines.
Furthermore, the ability of nociceptors to encode for the modality
of input alongside sensory information such as location, and
temporal and spatial patterning gives them a powerful influence
over the emotional and behavioural response. A sudden, stabbing
pain in the abdomen is a very different emotional experience than a
slow throbbing pain in the toe, even in the absence of top-down
information about what the pains might signify, and these varying
emotional experiences are largely shaped by the different primary
afferent information received. Even when previous knowledge and
top-down cognitive and emotional responses modify pain, these
top-down influences are largely limited by the information
specified by peripheral input. An individual prone to heartburn
might recognize a burning sensation in the chest as a signal to
take antacid, but might become more alarmed about the possibility
of a heart attack if they experience a more severe squeezing
feeling around their heart that spreads to their arms and neck. As
this example demonstrates, top-down processing associated with
cognitive, emotional and behavioural responses is largely selected
based on bottom-up signals encoding location, temporal patterning
and intensity.
The importance of this nociceptive input in shaping the
emotional response to injury (or potential injury) becomes readily
apparent when that input is compromised or unavailable. Individuals
with Nav1.7 sodium channel deletions (resulting in blocking of
primary afferent
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nociceptive input) are congenitally insensitive to pain.(Minett
et al., 2012) A recent interview with one such patient (“AR”)
demonstrated how different the response to potential injury is when
it is generated in an entirely top-down manner. At one point during
testing with noxious laser stimulation, AR calmly stated that “we
should probably stop, my hand feels like when I used to burn it
with a lighter”. Through previous experience (possibly
demonstrating to peers his ability to stoically endure fire?), AR
had learned what pattern of innocuous sensations were associated
with injury. In another example, AR described “the last time I
broke my ankle” (indicating how frequently such individuals sustain
serious injuries because of lack of peripheral nociceptive
responses) and how he had to rely on input from other sensory
modalities (the sound of bone cracking, the sight of displaced
bone, the feeling of blood flowing to the area) to become aware of
the injury. These descriptions are illuminating in two respects:
first because they demonstrate that in the absence of nociceptive
input, defensive responses to potential injury are entirely reliant
on learning (necessitating a history of injuries before learned
responses can become effective). Secondly, both descriptions were
noteworthy for their emotionally neutral tone. AR recalled the
cracking and displacement of his ankle in an emotionally blunted
manner more appropriate for reciting a bus schedule. Similarly, the
potential for a burn to the hand elicited a verbal response that
was devoid of any sense of threat or emotional urgency. It is clear
that in the case of pain, having highly specific information
available at the level of primary afferent is critical to pain’s
role as an unlearned warning signal, alerting the organism to
immediate somatic threat and facilitating appropriately urgent
responses.
In considering specificity of primary afferent input from the
periphery, however, Melzack and Wall(Melzack & Wall, 1965) make
a critical distinction between physiological and psychological
specialization. Physiological specialization is the assumption that
receptors differ in the lowest threshold at which they can be
triggered by a particular form of energy. Given the evidence cited
above, physiological specialization is generally accepted.
Psychological specialization is the further claim that each
psychological experience of the body must have a specific receptor,
which is both necessary and sufficient for that experience. In the
case of pain, this latter assumption is contradicted by a variety
of phenomena where pain does not correspond with the level of
nociceptive input from the area where pain is experienced. These
include referred pain (pain that is experienced in a site other
than injury, as when arm or shoulder pain is experienced during a
heart attack), episodic analgesia (where pain is not felt
immediately after injury due to demands of the context of injury),
phantom limb pain, and allodynia (pain elicited by a stimulus not
intense enough to trigger nociceptors).
IS THERE SPECIFICITY AT THE LEVEL OF THE BRAIN?
Since the first neuroimaging studies of pain,(Davis, Wood,
Crawley, & Mikulis, 1995; Jones, Brown, Friston, Qi, &
Frackowiak, 1991; Talbot et al., 1991) hundreds of studies have
used functional neuroimaging to examine the response to acute
nociceptive stimuli. As identified by several
meta-analyses,(Apkarian, Bushnell, Treede, & Zubieta, 2005;
Duerden & Albanese, 2013; Farrell, Laird, & Egan, 2005)
these studies identify a pattern of neural activation common across
nearly every study. Areas responding to pain include anterior
cingulate cortex, insula, thalamus, primary and secondary
somatosensory cortices and motor and premotor regions. Due to the
ubiquity of their activation in pain studies, these regions came to
be known as the “pain matrix” and have been considered a potential
biomarker for pain in medical and legal settings.(Reardon, 2015)
The specificity of these regions has been called into question,
largely in response to a line of research into “social pain”.
Foundational studies(Eisenberger, Lieberman, & Williams, 2003;
Kross, Berman,
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Mischel, Smith, & Wager, 2011) in this area observed
activation in “pain matrix” regions when individuals experienced a
sense of social exclusion. These studies have played an important
function in drawing attention to the potential overlap between
neural systems responsive to nociception and to other emotionally
evocative experiences and outlining potential evolutionary
mechanisms responsible for this overlap.(Macdonald & Leary,
2005) A more controversial interpretation of this work, however,
and one that has been particularly prevalent in accounts of this
work in the popular press – is that this potential mechanistic
overlap implies experiential overlap. In other words, that pain
matrix activation suggests that social exclusion “hurts” (i.e.
feels like the emotional response to tissue damage). Given that
social stimuli are not associated with nociceptive input, such a
claim would undermine the role of nociceptors in guiding the
specific emotional experience of pain. Evaluating this claim
requires asking whether activation of the “pain matrix” is
sufficient evidence for the presence of pain. Downar and Davis and
colleagues(J. Downar, Crawley, Mikulis, & Davis, 2000; Jonathan
Downar, Mikulis, & Davis, 2003) first called the specificity of
these responses into question in an early series of fMRI
experiments, demonstrating that a network of regions largely
overlapping the pain matrix were associated with the novelty and
relevance of environmental stimuli rather than their painfulness.
Following on from this work, Mouraux and colleagues(A. Mouraux
& Iannetti, 2009; André Mouraux, Diukova, Lee, Wise, &
Iannetti, 2011) demonstrated “pain matrix” activation in response
to salient (but non painful) stimuli in other sensory modalities
(visual, auditory, non-painful tactile). It has been argued that
such studies do not necessarily demonstrate that “pain matrix”
responses are non-specific, since pain is not explicitly measured
and it can therefore not be ruled out that “a non-nociceptive
pricking sensation or a very loud noise could be experienced as
painful”.(Eisenberger, 2015)
To test this possibility we have recently tested neural
responses to noxious mechanical stimulation in two patients
congenitally insensitive to pain due to a deletion in the NaV1.7
sodium channel. These individuals’ responses to tactile stimulation
are fully intact and their ratings of sensation were comparable to
those of healthy controls. Thus, the stimuli were fully matched for
both physical and perceptual stimulus intensity and only differed
in the presence of perceived pain. The congenitally insensitive
patients had robust “pain matrix” activation, equivalent to that of
healthy controls (see figure 2). These studies demonstrate that
“pain matrix” activation is not sufficient evidence for the
presence of pain.
Recent evidence further suggests that an intact “pain matrix” is
not necessary for pain perception. We have demonstrated intact pain
responses (using multiple dependent measures including pain
ratings, psychophysiological responses, facial action coding and
verbal reports) in an individual with extensive damage to the “pain
matrix” (including near-complete ablation of the anterior cingulate
and insular cortices) as well as key limbic structures like the
amygdala.(Feinstein et al., 2010, 2015) These findings, together
with previously mentioned studies demonstrating “pain matrix”
activation in response to non-painful stimuli, seriously call into
question whether the “pain matrix” is either necessary or
sufficient for the experience of pain.
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FIGURE 2 The “Pain Matrix” in Pain-Free Individuals: (A) shows
the Neurosynth-based “pain matrix” (red) and the regions where all
control subjects had significant activation in response to noxious
stimulation (blue). (B) shows activation levels (z-scores) of
single subjects within regions of the “pain matrix” (C) shows the
Neurosynth-based “pain matrix” (red) and “pain matrix” regions
where pain-free individuals had significant activation (yellow).
(D) shows the conjunction (green) of pain-free and control
activations within the Neurosynth-based “pain matrix” regions.
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WHAT ROLE FOR THE BRAIN IN PAIN?
Does evidence for the non-specificity of the pain matrix suggest
that the brain plays a limited role in the perceptual experience of
pain? Perhaps there was some truth in Descartes’ original
conceptualization of the brain as a bell to be rung by a string in
the periphery? Perhaps there is no specific representation of pain
in the brain and it merely reacts as it might to any salient,
adaptively relevant stimulus?
Prior to evaluating this possibility, we must consider a more
mundane explanation for the lack of specificity observed in neural
responses detected in the neuroimaging literature, namely that
technical limitations make fMRI poorly suited to detect
pain-specific responses. The temporal resolution of fMRI (the most
popular of these techniques) is on the order of seconds, far below
the timescale of nociceptive input. Furthermore, fMRI relies on
oxygenated blood flow as a proxy for neuronal activation,
introducing temporal delays and further measurement imprecision.
Finally, the spatial resolution (in cubic millimetres) is too
coarse to differentiate between smaller populations of more
specialized neurons. Spatial resolution might be a particular
problem in understanding the role of ubiquitous “pain matrix”
regions like insula and ACC whose integrative role means several
types of neurons might exist in close proximity to each other.
Indeed, noci-responsive neurons have been found in both regions
using techniques with higher spatial resolution,(Frot, Faillenot,
& Mauguière, 2014; Frot, Mauguière, Magnin, &
Garcia-Larrea, 2008; Hutchison, Davis, Lozano, Tasker, &
Dostrovsky, 1999) suggesting that the non-specificity of
activations detected using fMRI (and other neuroimaging techniques
with equal or worse spatial resolution) might simply reflect
technical limitations that obscure differences between activation
driven by nociceptive responses from those driven by other types of
input.
It is also possible that the fMRI analyses being used are
sub-optimal in terms of detecting differences. GLM based univariate
analyses typically focus on single voxels, but employ spatial
blurring to account for non-independence of adjacent voxels. A
cluster-based thresholding technique is then commonly used to
determine whether a sufficient number of adjoining voxels reach a
threshold level of activation under a particular condition. Such an
approach largely ignores and even obscures the spatial pattern that
gives rise to overall activation within a particular cluster. Two
activation maps might therefore identify a common cluster, but
arising from different spatial patterns. Utilizing this spatial
information is the basis for a newer machine-learning technique
called multivoxel pattern analysis (MVPA), which seeks patterns of
activation that distinguish between conditions. This technique has
recently been used to demonstrate that sensory data in one modality
elicit characteristic patterns of activation in regions of primary
somatosensory cortex traditionally viewed as dedicated to other
sensory modalities.(Liang, Mouraux, Hu, & Iannetti, 2013)
MVPA has been used by Wager and colleagues(Wager et al., 2013)
to derive a “neurosignature” for pain. In a comprehensive set of
experiments, Wager and colleagues first established a
neurosignature that differentiated between four levels of perceived
pain. They then demonstrated that this neurosignature could
distinguish between painful and non-painful stimuli in an
independent data set. In a third experiment they used the
neurosignature to distinguish between social and physical pain.
Finally, they demonstrated the sensitivity of this neurosignature
to an analgesic agent (reminfentanil). In a follow up study, the
same group used MVPA along with a separate modifiability criteria
to demonstrate patterns of activation that exclusively
distinguished pain and social exclusion, further challenging the
neural overlap account of social and physical pain.(Woo et al.,
2014)
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The notion that emotional experiences that are perceptually
distinct from each other will have distinct neural representations
is intuitive; so it is tempting to conclude that these analytical
advances have succeeded in locating pain-specific circuitry in the
brain. It is important, however, to distinguish between empirical
and mechanistic specificity. If I look out the window in the
morning and can’t see whether rain is falling from the sky, I might
use other data to determine whether it is raining. I observe dark
clouds in the sky, people are wearing raincoats or walking with
umbrellas, there are rain puddles on the ground and passing cars
are using their windshield wipers. Intriguingly in this situation,
the measures that provide the greatest discriminative power (e.g.
windshield wipers) provide no information about how or why it
started to rain. In fact, we would learn most about how the rain
got there by examining the marker providing the least
discriminative power (dark clouds, which can be observed in many
different weather conditions). This analogy helps to illustrate the
distinction between empirical and mechanistic specificity. Markers
that are useful for discriminating one state from another may be
merely epiphenomenal, providing no information about the conditions
necessary for that state to exist. They provide empirical
specificity, but the degree to which we can infer mechanistic
specificity of any of the constituent regions remains an open
question. In the case of the MVPA derived pain signature, the
degree to which this distinction matters depends on what the
signature is being used for. For experimental purposes requiring a
quantitative measure of neural activity characterizing acute pain,
empirical specificity is enough. If, however, we want to better
understand how the brain gives rise to the specific experience of
pain (or, more specifically, evaluate whether empirical specificity
implies mechanistic specificity in the case of pain), these
findings are only a start. Moving towards a better understanding
will be aided by testing and corroborating models derived from
human imaging results with methods that allow for stronger causal
and directional inferences. These include studies in non-human
species where cell populations and circuitry can be modified, and
studies of individuals with relevant genetic mutations or
lesions.
As outlined in the previous paragraph, the fact that dark clouds
are causally linked to rain is not undermined by the fact that they
are not sufficient evidence that it is raining. Similarly the fact
that particular regions might be activated during mental states
other than pain (i.e. are not sufficient evidence for the presence
of pain) does not mean they aren’t involved in the generation of
pain. In fact, in evaluating the degree of mechanistic specificity
implied by empirically specific “neurosignatures”, Zaki and
colleagues(Zaki, Wager, Singer, Keysers, & Gazzola, 2016) point
out that these signatures may very well reflect patterns of neural
activation in a set of regions which individually may not be
specific to that state. This is clearly a pattern theory account.
Within this context, it is worth noting that in seeking patterns of
spatial activation specific to a state, MVPA and similar techniques
implicitly assume a pattern account of neural representation.
Given the evidence reviewed above, and the variable link between
nociception and pain, it seems doubtful that there is psychological
specialization for pain at any level of the nervous system. In
other words, there is no afferent neuron or brain region that is
both necessary and sufficient for the psychological experience of
pain. In terms of physiological specialization, however, extant
evidence suggests a distinction between the periphery and the
brain. There is strong evidence for primary afferents specialized
to detect stimuli intense enough to cause injury. As we ascend the
neuroaxis, however, physiologically specific transmission becomes
less prominent, beginning at the dorsal horn of the spinal cord,
the first relay between the periphery and brain. Some primary
afferent nociceptors synapse on nociceptive specific
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neurons (primarily in laminae I-II) but these are relatively
rare. More common are deeper-lying wide dynamic range (WDR) neurons
that receive afferent input from both A-delta and C fibers but also
from larger A-beta fibres sensitive to non-nociceptive sensory
input in various modalities.(D’Mello & Dickenson, 2008) In this
sense, though primary afferent input is largely specific to sensory
input able to cause injury (and pain), at the spinal cord and
above, this information is increasingly integrated with
non-nociceptive information. At the level of the brain, there is
little current evidence for physiological specialization. Rather,
neuroimaging provides stronger support for a pattern account, where
pain is represented across a network of regions, none of which is
specific to pain. Indeed, the two most ubiquitous “pain matrix”
regions – anterior cingulate and insular cortices – have been
implicated in a wide range of cognitive, affective and regulatory
functions.(Menon & Uddin, 2010; Shackman et al., 2011) Within
this context, it is noteworthy that the most prominent recent
update to the specificity account – Craig’s mechanistic account of
pain as a “homeostatic emotion” – places important limitations on
the degree of specialization in the brain. Based on compelling
anatomical evidence, Craig’s account posits lines that are largely
labelled for nociceptive input not only at the primary afferent
level, but from spinothalamic tract neurons originating from
laminae I. It is noteworthy, however that the brain regions viewed
as part of this mechanism (particularly at the cortical level) are
not viewed as pain-specific but, rather, as subserving the
regulation of a wider class of homeostatic functions (e.g. itch,
hunger, thirst, changes in blood pressure).
This arrangement, whereby nociceptive input is increasingly
integrated with other sensory, cognitive and affective information
at ascending levels of the neuroaxis serves an important adaptive
function. Information-rich input from the periphery allows for
defensive responses which require little higher order processing.
In fact, nociceptive flexion reflexes demonstrate that rudimentary
defensive responses can occur without any involvement from the
brain. An optimal defensive system, however, requires recognition
that some nociceptive input presents little danger (for example, an
experimental pain study in which the participant receives
well-controlled nociceptive stimuli and is assured that they will
not cause lasting damage) while some sub-nociceptive input might
represent grave threat to the body (e.g. a dull abdominal sensation
from a region where a malignant tumor has previously been removed).
Emotional responses can be generated simply by nociceptive input
but also by higher-order evaluations of the meaning of the input.
Fields has referred to these as primary and secondary affect,
respectively.(Fields, 1999) This combination of bottom-up and
top-down influences, whereby sensory input is sufficient to trigger
a “quick and dirty” emotional response that can be supplemented and
adjusted on the basis of top-down contextual evaluations is similar
to LeDoux’s account of adaptively critical emotions like
fear.(LeDoux, 1996)
Conclusion:
It is impossible to discuss the role for the body in forming the
emotional experience of pain, or to consider the implications of
this discussion for other emotional experience without re-visiting
the historical debate about specificity vs. pattern based
representation of pain. The evidence reviewed here suggests that
there is considerable physiological specificity at the level of
primary afferent input, but that this input becomes increasingly
integrated with other sensory and emotional information as it moves
up the neuroaxis. This arrangement allows for more nuanced
evaluation of threat but also introduces greater ambiguity, which
may,
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under some circumstances lead to maladaptive pain experiences
that do not accurately reflect specific threat to the body. Some
evidence supports the existence of nociresponsive neurons in the
brain. Nevertheless, it must be concluded that despite recent
analytical advances, neuroimaging has not provided strong evidence
for specific, dedicated circuits subserving pain processing.
Rather, pain representation in the brain appears to be an emergent
property of activation across circuits subserving processes common
to a broader class of adaptively salient stimuli.
In considering pain as a model for how an emotion might be the
product of specific input from the body, a question is whether it
serves as a model for all emotions or only for “homeostatic
emotions” whose primary adaptive function is to motivate action on
the basis of the state of the body. A primary role of pain is to
motivate withdrawal or other protective behavioural responses.
These are dependent on specific information about the somatic
location, intensity and temporal characteristics of a potentially
dangerous stimulus. Towards this end, it makes intuitive adaptive
sense to have rich data from dedicated fibers in the body to
facilitate “quick and dirty” responses (to use LeDoux’s
terminology). At higher levels of processing, it is important to
contextualize the information in light of other threats or safety
signals. In this sense, shared processing with other classes of
adaptively salient stimuli is not only efficient, but advantageous,
as it allows for more holistic judgements about threat and
appropriate response. Other emotions like sadness generally require
less specific information about the state of the body, so the
adaptive utility of highly specific somatic signatures is
questionable. Though pain has a high level of somatic specificity,
this specificity does not appear to be a necessary property of
other emotions but, rather, a reflection of the adaptive
motivational purpose that pain serves. Thus, instead of asking
whether emotions are specified in the body, we should ask whether a
particular emotion requires specific information from the body to
serve its adaptive purpose.
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