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Perspectives: The Nature of Feelings: Evolutionary and Neurobiological Origins
Perspectives: The Nature of Feelings: Evolutionary and Neurobiological Origins
can be used to guide physiological correc- monitored and centrally represented. From an evolutionary standpoint, the
tions. In the event of a disturbance, both A physiological deviation (for example, appearance of central maps of body states
the magnitude and spatial location of the hypoglycaemia) is sensed and centrally may have preceded the advent of the felt
deviation can be instantly monitored, and mapped, triggering corrective homeostatic experiential aspect that defines feelings.
the maps can be used both to trigger correc- changes (such as visceral motility and secre- This notion is supported by the finding that
tive actions, such as endocrine responses or tion, salivation, search for food, and so on). subjective, felt experience does not seem
emotive actions, and to suspend those cor- After feeding, the physiological deviations to be required in order for the maps to be
rections once equilibrium is regained. In the are corrected and the new parameters cen- used in the detection and correction of
case of hunger, aspects of the state of satiety trally mapped, triggering the suspension of homeostatic imbalances. In fact, numerous
(for example, glycaemia) are constantly the corrective measures29–32. disturbances are detected and dealt with
via action programmes or even simpler physi- stimulus triggers a concert of responses, Glossary
ological mechanisms without an accompany- including preparatory actions (such as Action programmes
ing conscious experience, that is, a feeling. increased heart and respiratory rates, anal- A set of innate physiological actions triggered by changes in
Examples of physiological processes that gesia or the secretion of cortisol), freeze the internal or external environments and aimed at
can occur subconsciously include regula- or flight behaviours (with immobility and maintaining or restoring homeostatic balance. The actions
include changes in viscera and internal milieu (for example,
tion of heart rate, modulation of endocrine impending motion, respectively, leading to
alterations in heart rate, breathing and hormonal secretion),
functions, adjustment of smooth muscle different arrangements of blood flow) and striated muscle (for example, facial expressions and
contraction, regulation of immunity, auto- attentional behaviours (leading to saliency running) and cognition (for example, focusing attention
nomic changes associated with the display of the causative object)5,49–53. and favouring certain ideas and modes of thinking). Action
of emotion-specific facial expressions, and From a bioengineering standpoint, the programmes include drives and emotions. Changes in body
state resulting from an action programme are sensed by
even some aspects of facial recognition and engagement of homeostatic action pro- the interoceptive system, displayed in sensory maps of the
decision-making 33–40. Our hypothesis is that grammes requires four elements. First, a com- body and may be experienced consciously as feelings.
the addition of a felt experiential component petent stimulus, such as an internal deviation
to the basic somatic mapping emerged and from homeostatic range or an external object Drive
An action programme that is aimed at satisfying a basic,
prevailed in evolution because of the benefits or circumstance, be it currently perceived or
instinctual physiological need. Examples include hunger,
it conferred on life regulation. Given that recalled in mind. Second, neural interfaces thirst, libido, exploration and play, care of progeny and
body states are necessarily valenced — they capable of detecting the stimulus. Third, neu- attachment to mates.
are either good or bad from the point of view ral execution sites capable of coordinating a
of homeostasis — feelings are powerful prox- collection of corrective actions — that is, the Emotions
Action programmes largely triggered by external stimuli
ies of ongoing biological value and natural action programme (drive or emotion). And (perceived or recalled). Examples include disgust, fear,
guides of adaptive behaviour. Feelings along fourth, neural interfaces capable of detecting anger, sadness, joy, shame, contempt, pride, compassion
a range that includes pain and pleasure at its the completion of the correction and halting and admiration.
extremes force the organism to attend to its the corrective actions5. In summary, inte-
current conditions. Feelings also facilitate grated neural maps of ongoing body states Ephaptic transmission
Sideways interneuronal communication that is mediated
learning of the circumstances surrounding provide an effective neural interface for the by extracellular current flow.
a change in body state and the subsequent detection of internal deviations from homeo-
application of this knowledge to the pre- static range (stimuli), for the triggering of cor- Feelings
diction of future situations, resulting in an rective responses (action programmes: drives The mental experiences that accompany body states.
Action programmes (drives and emotions) can elicit
increase in behavioural flexibility 5,41–43. In and emotions), for determining when such feelings. Experiences related to exteroceptive senses
brief, felt experiences permit more flexible corrective actions can be suspended and for (vision, hearing, touch, taste and smell) commonly cause
and effective corrective measures than neural generating the experiential component of the emotions and ensuing feelings but in general are not felt in
mapping alone, especially in the realm of mapped body states (feelings). and of themselves. This definition also excludes the use of
‘feeling’ in the sense of ‘thinking’ or ‘intuiting’.
complex behaviour 17,41.
The neural substrates of feeling Homeostasis
Drives/emotions facilitate homeostasis Neural processes can be studied at two main The process of maintaining the internal milieu physiological
The immediate goals of homeostasis concern levels: macroscopic (the systems level, which parameters (such as temperature, pH and nutrient levels)
the management of life processes, includ- is composed of general brain regions) and of a biological system within the range that facilitates
survival and optimal function.
ing the governance of metabolism and the microscopic (neurons, synapses, glia
maintenance of somatic integrity via self- and their molecular components). Thus, Interoceptive system
repair and defence44. Action programmes are cognition can be analysed at the level of A collection of nerve pathways and CNS nuclei dedicated
instrumental for achieving these goals45. brain nuclei, regions or lobes, but its roots to detecting and mapping homeostatic signals (such as
degrees of visceral muscle contraction and internal milieu
Action programmes do not require are ultimately found at the level of neuronal
chemical composition). The main interoceptive pathways
deliberation. They are instinctual — that is, networks and the intricacies of synaptic are the vagus nerve and the lamina I (spinothalamocortical)
biologically pre-set and largely stereotypical. signalling 21,54,55. Similarly, it is conceivable pathway. The interoceptive system monitors the state of
For example, in the case of pressure from a that feelings also include both macro- and the body, orchestrates responses thereto and has a central
sharp object, the ensuing action programmes microscopic-level neural substrates56. There role in generating feelings.
include retraction of the affected area away is remarkable evidence available regarding
from the stimulus and facial muscle contrac- the macroscopic analysis of feeling states, regions have been implicated: nucleus tractus
tion to form an expression of pain. However, and some preliminary proposals can be solitarius (NTS); area postrema; parabra-
their deployment can be influenced by learn- advanced. We therefore begin the search for chial nucleus (PBN); ventral tegmental area
ing (conditioning), which also allows the the neural substrates of feelings at the level (VTA); other monoamine nuclei; substantia
extension and transfer of homeostatic goals of macroscopic brain regions. The cellular nigra and the red nucleus; periaqueductal
to objects and situations that become imbued basis of feelings, by contrast, is barely begin- grey (PAG); the deep layers of the superior
with biological value: for example, money, ning to be approached. We discuss it in the colliculus (SC); and the hypothalamus5,42,61–63.
power or drugs46,47. last section. The intrinsic nature of these nuclei differs
The action programme of fear provides Prior research in the mammalian brain considerably, although they are all involved
another emblematic illustration of this has implicated a number of regions in the in generating corrective homeostatic actions.
process. The trigger for fear can be external generation of drives and emotions that sub- The PBN, NTS, PAG and SC display obvi-
(such as a threat) or internal (such as an sequently lead to feelings. These regions can ous topographic maps of body states5,61,64–72,
evolving myocardial infarction or air hun- be found at all levels of the neuraxis57–60. In whereas the VTA, other monoamine-secreting
ger owing to oxygen restriction)45,48. The the brainstem, for example, the following nuclei and the substantia nigra do not appear
to contain topographically organized infor- (FIG. 1). The lamina I spinothalamocortical metabolism and water balance, and are posi-
mation pertaining to the body. In keeping pathway is an afferent pathway convey- tioned along the surface of the brain ventri-
with the notion that feelings are likely to arise ing both thermo-algic and chemosensory cles, where neurons make direct contact with
from maps of body states, it is sensible to information from most tissues of the body the cerebrospinal fluid owing to the lack of
focus the search for neural substrates of feel- to the spinal cord (lamina I of the superfi- a blood–brain barrier 88. One such organ is
ings on the regions exhibiting topographically cial dorsal horn) and brainstem (trigeminal the area postrema, a chemosensing nucleus
organized somatic maps. nucleus)4,79–84. The vagus nerve, which is the adjacent to the NTS.
A set of structures located within the main conduit for visceral sensation, carries Interoceptive information gathered in
subcortical grey — including the amygdala, signals pertaining to visceral states — espe- the spinal cord and lower brainstem con-
nucleus accumbens, ventral striatum, ven- cially from the cardiovascular, respiratory, verges in higher brainstem regions, such as
tral pallidum and other basal ganglia and gastrointestinal and genito-urinary systems the PBN, the PAG and the reticular forma-
basal forebrain sectors — are involved in — to the NTS in the lower brainstem85–87. tion4,61,89 (FIG. 1). The PBN, PAG and reticular
generating homeostatic actions, ranging Additional structures involved in interocep- formation are closely and bidirectionally
from valence modulation (for example, taste tion are the circumventricular organs. These interconnected90–92. Interoceptive informa-
hedonia in the nucleus accumbens73) to the are specialized structures that are involved tion originating from different parts of the
triggering of motor behaviours (for example, in homeostatic functions, such as energy organism is continuously monitored and
fight or flight responses by the amygdaloid
nuclei49,52,53). These regions do not appear to
exhibit topographic maps. Thus, they may Cerebral cortex Other cortical areas
not have a direct role in generating feelings
but instead may help shape the state of the
body, for example via action programmes.
At the level of the cerebral cortex, several Anterior Posterior
candidate structures need to be considered. insula insula
The insular and somatosensory cortices (SI
and SII) have fine-grain topographically Thalamus
organized maps of the body, and are thus Thalamic nuclei
likely to provide direct substrates of feel-
ing 4,60,74. The anterior cingulate cortices also Brainstem Hypothalamus
exhibit a mapped organization, although
PAG SC
their more noted function is the generation
of actions. For example, motor responses to
pain can be initiated in the anterior cingulate PBN
cortex 75–77.
In brief, the most prominent system level AP NTS
Lamina I
topographically mapped within these struc- Specifically, complete bilateral destruction compelling evidence for a role of subcortical
tures61,64–67. Thus, the upper brainstem (that is, of the insula as a result of herpes simplex structures. Decorticated mammals exhibit
the PBN and PAG) is the most caudal site at encephalitis does not abolish either body or a remarkable persistence of coherent, goal-
which different aspects of interoceptive affer- emotional feelings, including pain, pleasure, oriented behaviour that is consistent with
ent information can be assembled to form a itch, tickle, happiness, sadness, apprehen- feelings and consciousness112. Moreover,
whole-body, integrated map of body states. sion, irritation, caring and compassion, in electrical stimulation of certain regions of
Such a map has a crucial role in life regula- addition to hunger, thirst, and bladder and the brainstem can elicit behavioural mani-
tion and, in all likelihood, simultaneously colon distension114 (FIG. 2). In fact, feelings festations that are consistent with emotional
provides a neural basis for the emergence of seem to dominate the mental landscape responses in mammals. These responses are
feeling states. of patients with bilateral insular damage. imbued with positive and negative valence
The SC warrants a special note. Although Immediate comfort appears to be their in accordance with the type of emotion
the role of its ‘superficial’ layers (layers I to main concern, fairly unbridled by cognitive elicited and as determined by their effect
III) in vision is well established93, the ‘deep’ constraints. on learning a simple task or the voluntary
layers (layers IV to VII) have been relatively These observations do not support a view switching on or off of the stimulus by the
overlooked despite their physiological rel- of the insula as a necessary substrate for feeling animal42,117. Electrical stimulation of the
evance. The deep layers of the SC receive states. Thus, the generation of feelings must brainstem can also elicit both emotions and
inputs from different modalities (visual, also rely on the brainstem and possibly on the the corresponding feelings in humans118.
auditory and somatosensory), resulting in SI and SII somatosensory cortices of the pari- Together, these findings indicate a key role
three superposed topographic maps in a etal lobe, which are spared in some patients of the brainstem in triggering and support-
spatial register (that is, a region of one map that lack the insular cortices but remain fully ing emotion and feeling.
corresponds to a specific region of the other capable of feeling114. Indeed, damage to the Normal human feelings do not require
two) so that there is correspondence between posterior half of the upper brainstem is asso- the insula, although they consistently engage
the information contained in all three ciated with coma or vegetative state — two this region. To reconcile these observations
maps94–97. This unique arrangement suggests conditions in which feelings and sentience requires the consideration that the larger
that exteroceptive and interoceptive afferent are abolished. The nuclei located in this sec- maps of body state within the insula prob-
information may first converge in the SC to tor include some of the structures that con- ably permit the assembling of finer-grain
form an integrated sensory map. The SC has tain integrated somatosensory maps — the representations of interoceptive information
been implicated in visual attention98 and may PBN, PAG and SC — as well as the reticular than the maps assembled in the brainstem.
also play an important part in processes of formation and some monoamine and ace- In fact, some afferent information does
mind and self 42,99. tylcholine nuclei. By contrast, lesions of the appear to reach the insula directly, bypassing
ventral half of the upper brainstem cause the brainstem89. Information that is present
Feelings and the insula. Interoceptive infor- locked‑in syndrome, in which feelings and in the brainstem in implicit form may be
mation mapped in the brainstem is projected consciousness (from sentience to autobio- explicitly represented in the insula accord-
rostrally to the subcortical basal forebrain graphical levels) are not abolished17,115,116. ing to body coordinates provided by SI and
and to the cortical telencephalon, where it is Neuroimaging studies also suggest a link SII. Cortical re‑mapping would allow finer
remapped in the insula and somatosensory between feelings and the brainstem, because discrimination of interoceptive states and
cortices SI and SII4,17,58,84,100. inducing feelings triggers activation of permit a more precise modulation of the
Contemporary neuroscience has brainstem structures58,63. Research involving regulatory responses to an imbalance. In
identified the insula as the main cortical experimental manipulation provides more other words, insular maps would have more
target for signals from the interoceptive
system4,58,60,101,102, and functional neuroim- Horizontal Coronal
aging studies consistently implicate the
human insula in both interoceptive and
emotional feelings58,60,84,100,103–110.
Recently, it has been proposed that the
insula is not merely involved in human Control
feelings but is their sole platform and, by
extension, the critical provider of human
awareness60,111. Several findings suggest
that this hypothesis is problematic. First,
given that several topographically organ-
ized nuclei of the upper brainstem, which
are obligatory relay stations for most signals
conveyed from the body to the insula, can Patient B
produce elaborate representations of multi-
ple parameters of body states, these regions
should not be excluded a priori as platforms
for feelings. Second, children born without Figure 2 | Patient B shows complete destruction of insular cortices in anatomical MRI scans.
cerebral cortex exhibit behaviours compat- Top row, control; bottom row, patient B. Red circles mark the insula; yellow circles mark the brainstem;
ible with feeling states112,113. Third, bilateral blue circles mark the basal forebrain region. Data from REF. 114 Nature Reviews
. Image | Neuroscience
courtesy of H. Damasio,
insular damage does not abolish all feelings. University of Southern California, USA.
of a modulatory than a generative role in the evolution117. Although it cannot at present in the range of 1–8 ms−1, as opposed to the
processing and experience of body states. be demonstrated that non-human species well-myelinated Aα and Aβ fibres, which
This is consistent with the finding that uni- are capable of feeling, as feeling states are conduct exteroceptive signals at speeds of
lateral insular lesions diminish thermal and by definition subjective and accessible only 14–60 ms−1 (REF. 129).
nociceptive discrimination4,119,120, whereas to the organism in which they occur, there The vagus nerve, a principal conduit
even complete bilateral insular destruction is no reason to assume otherwise. In fact, of fine visceral information, is also pre-
does not abolish the ability to feel. Moreover, because many non-human species have all dominantly devoid of myelin. In mammals,
by virtue of its cortical location at the cross- the neural substrates that are likely to be including humans, approximately 80% of
roads of numerous pathways involved in essential for the emergence of feeling, and fibres in the main vagus trunk are unmyeli-
higher cognition, the insula makes exten- exhibit behavioural manifestations that are nated130,131, and most of the remaining 20%
sive connections to cortical regions related consistent with feelings and emotion, the are poorly myelinated132. This predomi-
to memory, language and reasoning. This parsimonious assumption should be that nance of unmyelinated fibres is even more
suggests that although the insula is not feelings are present in these species. The dramatic in the vagal branches133. The vagus
necessary for experiencing feelings, it may sophisticated cognitive processes facilitated is unusual among the cranial nerves in its
be essential for the introduction of feelings by the complex cerebral cortex of primates high content of unmyelinated fibres134, and
into the flow of cognitive processes and thus — such as memory, language, reasoning fibre arrangement within the vagus is also
facilitate the crosstalk between cognition and imagination — probably contribute to particular (whereas unmyelinated fibres in
and feeling. Such crosstalk may be necessary more enriched and refined feeling states other cranial nerves tend to remain clus-
for the acquired rational control of drives than those found in species with simpler tered in the periphery, in the vagus they
and emotions, the absence of which would nervous systems. Nonetheless, the funda- appear evenly and uniformly distributed
favour simpler behavioural patterns domi- mental elements of body state mapping, throughout the axonal substance134). Of
nated by feeling states. sentience and feelings imbued with valence note, unmyelinated fibres also mediate the
are likely to be far older than our species, affective aspects of touch78,135. The subset
Feelings and the somatosensory cortex. and probably even older than the advent of C fibres related to this function operates
With regard to the somatosensory cortices, of cerebral cortices. There is good reason as an additional component of the intero-
both SI and SII can be functionally engaged to believe that the primate brain inherited ceptive system. In addition to the afferent
during feelings58,121,122, but damage to the the neural instruments for feeling from its interoceptive pathways, the central relays
somatosensory cortices has little or no ancestors and elaborated upon them. receiving these signals — the area postrema,
effect on nociception and thermosensa- NTS, PBN and PAG — are also poorly
tion123. Moreover, both rhesus monkeys The cellular basis of feelings myelinated136–138.
and humans with bilateral parietal lesions What are the cellular correlates of feelings? Given that the classically accepted evo-
(encompassing both SI and SII, albeit not With rare exceptions, the issue has not been lutionary advantage of myelin sheaths is
in their entirety) exhibit behaviours clearly considered by the research community 5,54,56,127. the acceleration of impulse propagation
indicative of feeling states and display dra- However, we believe this effort is impera- along the axon139, one should question why
matic emotional lability 124,125. Although tive. The emergence of feelings requires the the critical systems involved in homeosta-
further evidence from cases of complete, intricate interplay between its macro- and sis have remained largely unmyelinated.
bilateral damage to both SI and SII is microscopic roots, both of which must be Myelination dramatically improves meta-
needed, the available evidence indicates that thoroughly elucidated if feelings and con- bolic efficiency during axonal conduction,
the somatosensory cortices are not neces- sciousness are to be fully understood. largely owing to a redistribution of ion
sary for the generation of body or emo- With regard to the microscopic or cellular channels — in myelinated fibres, these
tional feelings. Instead, it is likely that these substrate for feeling states, we propose that: are concentrated in the nodes of Ranvier
regions have a modulatory role in the expe- the crucial cells are to be found in the intero- rather than equally distributed along the
rience of interoceptive body states, similar ceptive system, specifically in the unmyeli- axon — and smaller ionic imbalances fol-
to that of the insula.
nated axons conveying signals from humoral lowing nerve conduction139,140. However,
and visceral aspects of the body towards owing to the metabolic price of generating
The evolution of feelings. Implicating sub- nuclei in the spinal cord and brainstem. We and maintaining myelin sheaths, myelina-
cortical regions such as the upper brainstem also suggest that the ephaptic signalling that tion may only be energetically profitable
and hypothalamus in the generation of feel- is likely to occur among such unmyelinated above a certain fibre diameter 141. One
ings has resounding evolutionary implica- axons has an important role. possible explanation for the persistence of
tions. Non-human mammals, birds, reptiles unmyelinated nerves is that only relatively
and even phylogenetically older species The processing of body signals largely relies thick fibres justify the metabolic cost of
clearly display behaviours that are consist- on unmyelinated structures. The intero- myelination, whereas fibres below a certain
ent with emotions and feelings5,42,43,126. ceptive pathways that are known to play a threshold remain unsheathed142. Another
Although there are dramatic differences part in feeling states generally display very possibility is that conduction speed is
between these species and humans at low levels of myelination. For example, the essential for certain neural processes but
the level of the cerebral cortex, the evo- lamina I spinothalamocortical pathway is not others, and the organism is willing to
lutionarily older brainstem is essentially comprised of small-diameter, unmyelinated pay the metabolic cost of myelination only
conserved in its layout, design and func- (C) and lightly myelinated (Aδ) fibres that when necessary. However, this explanation
tions. It is therefore justifiable to propose are encased in Remak bundles, in which implies that processes mediated by unmyeli-
that feelings are not exclusive to humans a single Schwann cell envelopes several nated fibres, such as nociception and basic
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