Disgust: Sensory Affect or Primary Emotional System?
Disgust: Sensory Affect or Primary Emotional System?
Cognition & Emotion, 2007, in press
Judith A. Toronchuk
Psychology and Biology Departments,
Trinity Western University
.and
George F. R. Ellis
Mathematics Department,
University of Cape Town
Running Head: Disgust: Sensory Affect or Primary Emotional System?
Contact information:
Psychology Department, Trinity Western University
7600 Glover Road, Langley, B.C. V2Y 1Y1 Canada.
Phone: 604-888-7511 extension 3104
email address: toronchu@twu.ca
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Disgust: Sensory Affect or Primary Emotional System?
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Abstract
We argue in this paper for the inclusion in the primary emotional systems enumerated by
Panksepp of a neural system which organises disgust responses. The DISGUST system
arose phylogenetically in response to danger to the internal milieu from pathogens and
their toxic products. We suggest that the primitive emotive circuit which originally
provided defence by regulating consummatory behaviours gave rise to a primary
emotional system which facilitates evaluation of reinforcers. Unlike the sensory affect of
distaste from which it is experimentally dissociable, disgust responses can involve
flexible learned components triggered by several modalities. The anterior insula is
implicated as playing a major role in the DISGUST system both in organizing disgust
responses in the individual and recognizing disgust responses in others.
Disgust: Sensory Affect or Primary Emotional System?
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Introduction
In this paper we present arguments for the inclusion of DISGUST 1 as a primary
emotional system, to be included in the list of such systems in addition to those
characterised as such by Panksepp (1998). Although numerous authors have established
lists of criteria for characteristics of basic emotions, Panksepp’s criteria are particularly
valuable in calling attention to the phylogeny of neural pathways. Using his
differentiation between sensory affect and primary emotional system, we wish to argue
that the complex, action-oriented affective response of the DISGUST system should be
distinguished from the sensory affect of “distaste”. According to Panksepp (1998, p.48ff;
see also Panksepp, 2000) six neurally-based criteria for primary emotional systems are:
1) genetically predetermined circuits accessible to various sensory stimuli, 2) the ability
to organize diverse behaviours, 3) the ability to change the sensitivities of relevant
sensory systems, 4) the use of feedback circuits to sustain arousal which outlasts
precipitating events, 5) modulation by cognitive inputs, and 6) modification and
channelling of cognitive abilities. In this scheme, a sensory affect is a sensation infused
with affective qualities and more related to perception than to emotion, while primary
emotions are action-orientated responses arising from “distinct emotional operating
systems that are concentrated in subneocortical, limbic regions of the brain” (Panksepp,
2005). While distaste seems to us to belong to the former category, we suggest the
DISGUST response belongs to the latter category and is a phylogenetic development
arising from mechanisms which originally functioned to prevent disease. We support this
claim below by arguing in turn for its phylogenetically ancient origins, activation by
diverse sensory modalities, ability to organize diverse behaviours, distinct neural
Disgust: Sensory Affect or Primary Emotional System?
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circuitry, ability to produce changes in hedonic value, arousal which outlasts precipitating
events, and modification and channelling of cognitive abilities
Phylogenetically ancient origins
While psychologists have long agreed in principle with the idea that emotions
have evolutionary origins and facilitate adaptive actions, most emotion researchers
(Panksepp is a refreshing exception) begin with human subjective experience and then
search for ad hoc supporting data from the mammalian order. In our thinking a wider
phylogenetic approach to the study of emotions such as that described by Lawrence and
Calder (2004, p. 16) is appropriate, except that we would not simply advocate a
mammalian perspective, but one which considers the entirety of vertebrate evolution.
We propose that the basic emotion referred to in humans as disgust evolved from the
reflexive distaste response of vertebrate ancestors, which in turn arose from primitive
chemosensory mechanisms originally adapted to avoid pathogens and their toxins.
Whether or not the use of the word `disgust’ should be limited to humans is not our
concern in this paper; rather our purpose is to explicate the evolution of a basic neural
operating system (DISGUST) which enables emotional responses to potentially
infectious, or noxious material, in advance of actual contact with such material. In
humans the basic emotion of disgust comes to be elaborated by higher cortical processing
not available to other organisms to include social status and moral concerns.
Natural selection requires that all organisms, no matter how simple, defend their
bodies against others. The problem of defence requires two basic systems: one to defend
against external threat and one to defend the internal milieu from toxins (Garcia,
Disgust: Sensory Affect or Primary Emotional System?
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Hankins, & Rusiniak, 1974; Garcia, Quick, & White, 1984, p. 49). All organisms must
protect themselves not only from external predators but also from invasive microorganisms and parasites within their own bodies as well as ingested toxic substances. The
learned avoidance of toxic or infected material before ingestion, as opposed to spitting or
vomiting after ingestion, would thus serve a useful adaptive function.
Throughout evolution danger to the internal milieu has been signalled by
chemosensory detection mechanisms found in all multicellular animals. Even sponges
and coelenterates, with rather limited behavioural repertoires, have within their bodies
wandering phagocytic amoebocytes which play a dual role in both nutrition and defence
from pathogens (Horton & Ratcliffe, 2001, p. 211). The avoidance of tastes previously
paired with noxious substances or illness, first described by Garcia, has since been
demonstrated in a wide range of mammals, birds, reptiles, fish, and various invertebrates
(see Bernstein, 1999; Carew & Sahley, 1986; Garcia et al., 1974; Garcia et al., 1984).
Even the bacteria-ingesting nematode Caenorhabditis elegans exhibits a chemoreceptor
mediated response in which it selectively avoids in a radial maze specific pathogenic
strains after 4 hrs. exposure (Zhang, Lu, & Bargmann, 2005). Garden slugs which
previously ingested carrot juice will avoid it after one or two trials in which the juice is
followed by poison (Garcia et al., 1984, p.48). Pond snails acquire differential
conditioned taste aversion to either sucrose or carrot juice paired with lithium chloride
(LiCl; Sugai, Shiga, Azami, Watanabe, Sadamoto, Fujito, et al., 2006). While we do not
suggest that these invertebrate examples represent the emotion of disgust, we do wish to
point out that they are the evolutionary precursors of the fully developed human emotion
of disgust.
Disgust: Sensory Affect or Primary Emotional System?
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Rozin and his colleagues have suggested the phylogenetic origin of disgust lies in
the distaste/oral rejection response of animals to bad tasting food (Rozin & Fallon 1987;
Rozin, Haidt, & McCauley, 1999). They hold the specifically human emotion of disgust
differs from the sensory distaste response of animals by the addition of concepts of
offensiveness, in particular those aroused by reminders of our animal nature. Further
human elaborations would include interpersonal and socio-moral disgust. More recently
Curtis and Biran (2001) have argued for evolutionary origins in more general protection
of organisms from infection. This latter theory is supported by the results of a massive
international survey (Curtis, Aunger, & Rabie, 2004) showing that disgust is universally
elicited by disease-salient contact stimuli such as bodily secretions, viscous substances,
vermin and sick or dirty people. A recent study on odour also supports the disease model
(Stevenson & Repacholi, 2005). Rubio-Godoy, Aunger and Curtis (2007) further suggest
disgust is a neural system “evolved to detect reliable signals co-occurring with diseasecausing infectious agents, which stimulates avoidance responses and/or other behaviours
that tend to decrease the risk of disease.” We propose touch, olfaction and taste were all
involved in the evolutionary development of the DISGUST system as early aquatic
vertebrates likely had in common with many modern fish wide-spread chemoreceptors on
their body surface, an adaptation which allows not only avoidance of ingestion but even
earlier avoidance of contact with infectious or noxious substances.
Activation by diverse sensory modalities
The first of Panksepp’s original criteria for an emotional system is that it be
controlled by a distinct neural circuitry unconditionally accessed by various sensory
stimuli (Panksepp, 1998, p. 48). Although taste may be the phylogenetically first, and
Disgust: Sensory Affect or Primary Emotional System?
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thereafter most prominent cue for aversion responses, other sensations can also be
effective triggers. In humans taste, olfactory, auditory, tactile and visual cues are all
capable of eliciting disgust (Curtis & Biran, 2001; Curtis et al., 2004). In mammals that
hold food in their front paws, aversions can develop to tactile and olfactory features of
the food (see Domjan, 2005). Visual cues such as the colour of monarch butterflies may
be associated by birds with illness; and according to Garcia’s group (1984, p. 57), avians
which eat relatively tasteless seeds also make excellent colour-illness associations, unlike
mammals which tend to make primarily taste-illness associations. Using colour cues,
birds avoid seeds associated with illness under conditions in which taste cues would be
less useful.
Miller (1997, p.169) notes that although the word disgust did not enter English
until the 17th century along with the aesthetic notion of “good taste”, its etymological
origin has likely biased English-speaking researchers to focus on the sensation of taste.
The lack of gustatory connotations in German Ekel and widerlich may have inclined
Freud to focus more on other sensory modalities (W. Miller, 1997 p.1; also S. Miller,
2004, p.12). Miller, rejecting a sole origin for disgust in taste elaborates, “Touch is the
world of the slimy, slithery, viscous, oozing, festering, scabby, sticky, and moist” (W.
Miller, p.19). Avoiding contact with infectious substances provides greater safety than
merely avoiding ingestion.
The selective activation of the DISGUST system (Garcia et al., 1974; Rozin &
Kalat, 1971) by only certain stimulus categories may be similar to “belongingness” or
“preparedness” of fear responses. Öhman and Mineka (2001) argue from the
“preparedness” of humans to fear certain stimuli such as snakes, spiders and angry faces
Disgust: Sensory Affect or Primary Emotional System?
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for the existence of an evolutionarily adapted fear system that organizes human fear and
fear learning. This system would respond more easily to stimuli which were important for
survival in the environment of our ancestors than to modern dangers such as guns; and it
would influence the ease with which fear associations are learned. The parallel manner in
which tastes seem prepared to activate disgust and the ease with which disgust may be
associated with taste suggests a similar argument for an evolutionarily adapted DISGUST
system.
Garcia and his colleagues (1984, p.51) have shown the visual appearance of a
food pellet can be associated by rats with shock but not with illness, whereas flavour can
be easily associated with illness but not with shock. The effectiveness of odour as a
stimulus for rats depends on the context. Odour alone is a good cue for association with
shock but not with illness, whereas odour plus taste can be easily associated with illness
but not with shock. When odour has been paired with taste during acquisition, odour
alone can then become a potent cue for aversion. It is commonly accepted that humans
also readily associate tastes with nausea (see Bernstein, 1999; Rozin & Fallon, 1987).
Ability to organize diverse behaviours
Responses of the DISGUST system can involve flexible voluntary components,
thereby satisfying another of the criteria for basic emotional systems (Panksepp, 1998,
p.49). Rats do not just avoid food items after taste aversive conditioning—they gape,
open their mouths, gag and retch, shake their heads, and wipe their chins on the floor. A
coyote may retch, roll on the offensive food and then kick dirt on it, while a cougar may
shake each paw. Monkeys may react to offensive objects by excessive sniffing and
manipulation often followed by breaking and squashing the item, then dropping or
Disgust: Sensory Affect or Primary Emotional System?
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flinging it away and wiping their hands (Garcia et al., 1984, p.57). The complexity of
these responses suggests they involve more than reflexes.
Certain immune and endocrine responses may also be activated as part of the
DISGUST system. Pairing of saccharine and a bacterial antigen can induce a conditioned
taste aversion (CTA) in rats along with a conditioned increase in both immune function
(interleukin-2 and interferon-γ) and corticosterone (Pacheco-López, Niemi, Kou, Härting,
Del Rey, Besedovsky, et al., 2004; also Alvarez-Borda, Ramirez-Amaya, Perez-Montfort,
& Bermudez-Rattoni, F. 1995; Ramirez-Amaya & Burmudez-Rattoni, 1999). This lends
credence to Curtis’ disease theory, especially in light of the fact that it is the immune
system that actually triggers malaise, fever, and other sickness behaviours.
Although “each species reacts with its species-specific disgust pattern” (Garcia et
al., 1984, p.57), individual organisms vary the pattern according to the external
circumstances. An incident from the Garcia lab illustrates the extent of diversity during a
procedure designed to produce conditioned taste aversion in rats (Garcia et al., 1984, p.
53). Animals were trained to drink from a tube protruding from a nose cone covered with
filter paper impregnated with initially neutral odours. After becoming ill from LiCl paired
with a novel odour and a novel taste in the water, rats later avoided plain water when it
was presented with the conditioned odour. Garcia observed some of these rats claw out
the filter paper containing this apparently offensive odour, push the paper through slots in
the floor at the other side of the cage, and only then drink the water.
While humans also give complex voluntary disgust responses, some behavioural
components do have an involuntary nature. Disgust elicits specific autonomic responses
in humans including reduced blood pressure, heart rate deceleration, increased skin
Disgust: Sensory Affect or Primary Emotional System? 10
conductance (Stark, Walter, Schienle, & Vaitl, 2005; see also Critchley, Rotshtein, Nagai,
O'Doherty, Mathias, & Dolan, 2005; Rozin & Fallon, 1987), and changes in respiration
(Ritz, Thons, Fahrenkrug, & Dahme, 2005). The autonomic components may also be
generated by voluntarily produced facial expressions of disgust (Levenson, Ekman, &
Friesen, 1990). Disgust also elicits a unique, fairly universally recognized, facial
expression (Ekman & Friesen, 1986; see also Wolf, Mass, Ingenbleek, Kiefer, Naber, &
Wiedemann, 2005) which is even elicited in congenitally blind individuals (Galati,
Scherer, & Ricci-Bitti, 1997) and correctly interpreted by children born deaf (Hosie,
Gray, Russell, Scott, & Hunter, 1998). Some researchers (e.g. Ekman) have used the
existence of a universal facial expression as one criterion for inclusion as a basic
emotion. However because components of this particular expression can also be elicited
in anencephalic neonates (see Steiner, Glaser, Hawilo, & Berridge 2001), it does not
seem likely that the facial expression differentiates between the emotion of disgust and
the sensory affect of distaste. While suggesting the existence of an innate mechanism,
facial expression does not make an adequate criterion for an emotion.
Distinct neural circuitry
The existence across species of common neural structures involved in triggering
disgust reactions suggests a unified affective system with ancient origins which has
undergone recent elaboration in humans. Both the human disgust response and
conditioned taste aversions in animals depend on allocortical regions of the insula
consistent with the suggestion that primary emotions arise from emotional operating
systems concentrated in subneocortical, limbic regions of the brain (Panksepp, 2005).
Disgust: Sensory Affect or Primary Emotional System? 11
In mammals reflexive vomiting and retching is organized by central pattern
generators in the medulla under the control of the nucleus tractus solitarius (NTS) (see
Hornby, 2001; Lawes, 1990). There is however no single “vomiting centre” that may be
activated by electrical stimulation, suggesting that emesis, like feeding, is under multiple
levels of neural control (Lawes, 1990). . Caudal NTS receives visceral and immune
system input from the vagus (X th) nerve and input regarding blood-borne substances
from area postrema, while the rostral NTS receives taste input from cranial nerves VII,
IX and X. Taste and interoceptive inputs enter separate areas of NTS forming two
pathways which first come together in the insula (reviewed in Bermudez-Rattoni, 2004;
Craig, 2002; Saper, 2002; Spector, 2000). Some differences between primates and other
mammals are evident in the inputs to the insula which Craig (2002, 2005) argues allow
the development of a greater degree of self-awareness in primates. In rodents both taste
and visceral input is relayed via the pons to the thalamus and then to the insula (see
Saper, 2002). Visceral input reaches the amygdala via the pons (see Bermudez-Rattoni,
2004). Formation of a CTA in rats requires both the anterior insula (AI) and the amygdala
to be intact (Lasiter, Deems, Oetting, & Garcia, 1985; Bermudez-Rattoni, Grijalva,
Kiefer, & Garcia, 1986). However decorticate rats still prefer sucrose and reject quinine
(Kiefer & Orr, 1992) consistent with the idea that distaste is a sensory affect requiring
only lower levels of the brainstem, while the DISGUST programme requires
subneocortical limbic structures. The insula appears to be required for rodents to
recognize the taste as novel (Berman, Hazvi, Neduva, & Dudai, 2000), while the
amygdala signals the aversive visceral components of the nausea/illness (Miranda,
Ferreira, Ramirez-Lugo, & Bermudez-Rattoni, 2002). Lesions in the insula not only
Disgust: Sensory Affect or Primary Emotional System? 12
disrupt acquisition and evocation of CTA, but also of immune enhancement or
suppression conditioned by either taste or olfactory cues, while leaving normal immune
functioning intact (Ramirez-Amaya & Bermudez-Rattoni, 1999; Ramirez-Amaya,
Alvarez-Borda, & Bermudez-Rattoni, 1998).
In primates the input to AI is more direct than in rats and the amygdala appears to
receive both taste and visceral input from the insula (Mesulam & Mufson, 1982; Mufson,
Mesulam, & Pandya, 1981), rather than through subcortical connections from NTS as in
rodents (see Rolls, 1989). Craig (2002, 2005) has proposed that this more direct pathway
allows for greater cortical integration in humans of visceral components.
The insula itself has three cytoarchitectural regions—agranular (named for its
lack of layered granular cells), dysgranular and granular. The anterior insula, consisting
of agranular and the anterior portion of the dysgranular regions, developed
phylogenetically as a centre for processing exteroceptive chemosensory input. More
posterior dysgranular and granular regions act as visceral sensory cortex (Saper, 2002).
Although the cytoarchitecture of the insula in humans and other primates seems
comparable (see Flynn, Benson, & Ardila, 1999), the human insula may be involved in a
wider range of emotional behaviours as suggested by its richer interconnections to
orbitofrontal cortex.
The primate agranular AI is relatively undifferentiated allocortex (rather than
neocortex) containing two or three layers which are continuous with agranular
orbitofrontal cortex (see Flynn et al., 1999; Gottfried & Zald, 2005). This region, like the
adjacent orbitofrontal region, receives olfactory input and responds to olfactory stimuli
(Critchley & Rolls, 1996). In humans the homologous olfactory area is further rostral in
Disgust: Sensory Affect or Primary Emotional System? 13
the orbitofrontal cortex (Gottfried & Zald, 2005), although the agranular AI is also
activated by olfaction and taste (de Araujo, Rolls, Kringelbach, McGlone, & Phillips,
2003). Dorsal and caudal to the agranular area is the five or six-layered dysgranular
region which is intermediate in appearance between agranular allocortex and fully
formed mammalian isocortex (neocortex). In rodents the taste area is found here
(Cechetto & Saper, 1987) and electrical stimulation of dysgranular insula produces
gastric motility (Yasui, Breder, Saper, & Cechetto, 1991). Monkey neurons in AI respond
to taste, olfaction, vision, texture or temperature of food (see Rolls, 2005a).
Human neuroimaging studies show that AI is involved in coding taste sensation,
olfaction, the reward value of taste (Royet, Plailly, Delon-Martin, Kareken, & Segebarth,
2003; Small, Gregory, Mak, Gitelman, Mesulam, & Parrish, 2003; Small, Zatorre,
Dagher, Evans, & Jones-Gotman, 2001), and participates in more comprehensive
mapping of other aspects of interoceptive bodily states (see Saper, 2002). For example AI
is activated by conscious awareness of: thirst (Egan, Silk, Zamarripa, Williams, Federico,
Cunnington et al., 2003), hunger (Tataranni, Gautier, Chen, Uecker, Bandy, Salbe et al.,
1999), sexual arousal (Stoléru, Grégoire, Gérard, Decety, Lafarge, Cinotti et al., 1999),
and heartbeat (Critchley, Wiens, Rotshtein, Öhman, & Dolan, 2004).
The posterior insula consists of granular six-layered isocortex which receives
primarily somatosensory and enteroceptive inputs. In rats neurons responding to
gastrointestinal sensation are found just caudal to and overlapping with the taste area, and
a few cells respond to both taste and gastrointestinal sensation (Cechetto & Saper, 1987).
Imaging studies show the human posterior insula responds to visceral and muscle
sensations along with pain, itch, temperature, hunger, thirst, etc. (see Craig, 2002; 2003).
Disgust: Sensory Affect or Primary Emotional System? 14
Lesions of human AI impair both the experience of disgust and the recognition of
disgust in others (Calder, Keane, Manes, Antoun, & Young, 2000). Penfield found that
stimulation of insula in humans invokes unpleasant tastes, nausea, and gastrointestinal
sensations (cited in Flynn et al., 1999). Recordings with depth electrodes from ventral AI
(agranular and anterior dysgranular) produced responses to pictures depicting facial
expressions of disgust but not to other emotional expressions (Krolak-Salmon, Henaff,
Isnard, Tallon-Baudry, Guenot, Vighetto, et al., 2003). Stimulation through these
electrodes produced unpleasant sensations in the throat, mouth, lips and nose described
by one patient as “difficult to stand”.
Numerous imaging studies provide evidence for the role of AI in elicitation of
disgust either by odours or visual stimulation with disgusting objects, and also in
recognition of disgust in facial expressions of others (Hennenlotter, Schroeder, Erhard,
Haslinger, Stahl, Weindl, et al., 2004; Phillips, Young, Senior, Brammer, Andrew, Calder
et al., 1997; Schienle, Stark, Walter, Blecker, Ott, Kirsch et al., 2002; Shapira, Liu, He,
Bradley, Lessig, James, et al., 2003; Wicker, Keysers, Plailly, Royet, Gallese, &
Rizzolatti, 2003). However the insula is also activated during other negative emotions
such as fear, anger or sadness (Damasio, Grabowski, Bechara, Damasio, Ponto, Parvizi et
al., 2000; Lane, Reiman, Ahern, Schwartz, & Davidson, 1997; Liotti, Mayberg, Brannan,
McGinnis, Jerabek, & Fox, 2000; Morris, Friston, Buchel, Frith, Young, Calder et al,
1998; Schienle et al., 2002).
Although AI is clearly involved in human disgust, other regions of the forebrain
are also implicated in the DISGUST system. Not surprisingly given the role of the
amygdala in rodent CTA and its anatomical proximity to and rich connections with the
Disgust: Sensory Affect or Primary Emotional System? 15
insula, several imaging studies have reported activation of the human amygdala by both
pleasant and unpleasant tastes (O’Doherty, Rolls, Francis, Bowtell, & McGlone, 2001)
and also during evocation of disgust (Phillips et al., 1997; Schafer, Schienle, & Vaitl,
2005; Schienle et al., 2002; Schienle, Schafer, Stark, Walter & Vaitl, 2005). Studies of
Huntington’s, Parkinson’s and obsessive compulsive patients also suggest a possible role
for the basal ganglia in the DISGUST system (Sprengelmeyer, Young, Calder, Karnat,
Lange, Hömberg et al., 1996; Sprengelmeyer, Young, Mahn, Schroeder, Woitalla,
Büttner et al., 2003; Sprengelmeyer, Young, Pundt, Sprengelmeyer, Calder, Berrios et al.,
1997). The AI is therefore only one region involved in the processing of human disgust; it
is apparently a necessary region, but one which is also involved in other negative
emotions. Other functions of the human insula will be considered below.
Changes in hedonic value
The DISGUST system is able to produce changes in the hedonic value of tastes
consistent with the third criterion outlined above (Panksepp, 1998, p. 49; Panksepp,
2000). CTA can be elicited by tastes that would otherwise be pleasant, showing that CTA
is more than just distaste. CTA, as further discussed below, can be dissociated from
avoidance and can also be elicited by tastes that would otherwise be pleasant. This
suggests a change occurs in the hedonic value of the taste. Pelchat, Grill, Rozin and
Jacobs (1983) trained groups of rats to avoid sucrose either when paired with illness,
shock or lactose (rats are lactose intolerant). All groups learned to avoid sucrose, but only
those in which sucrose was paired with illness showed the orofacial aversion response
(gaping) indicating the preferred taste actually became aversive.
Disgust: Sensory Affect or Primary Emotional System? 16
Experiments by Kiefer and Orr (1992) confirm that CTA involves changes in
hedonic value. Lesions in the insular taste area (agranular and dysgranular) do not lead to
a failure of rats to dislike quinine or to like sucrose, but do lead to impaired learning of
taste avoidance accompanied by lack of aversive reaction to a taste paired with illness.
This suggests that mere avoidance does not entail a palatability shift whereas the insular
taste area is necessary for the shift in palatability that occurs in learned taste aversions.
Furthermore electrical stimulation of insula in anesthetised rats can modulate both
positively and negatively neural taste responses in the parabrachial nucleus (PBN) of the
pons (Lundy & Norgren, 2004), showing that there is a mechanism located in the insula
for downward modulation of gustatory responses.
When a novel taste is paired with LiCl, c-Fos expression is greater in the NTS,
PBN, amygdala and insula than when a familiar taste is paired with LiCl, whereas a novel
taste alone only increases expression in the amygdala and insula (Koh & Bernstein,
2005). Lesioning the insula eliminates the differences shown by rats exposed to these
three taste conditions (novel taste + LiCl, familiar taste + LiCl, novel taste alone)
suggesting changes in hedonic value are influenced by the insula. The insula modulates
both PBN and NTS, providing a mechanism whereby illness can affect the response of
these lower nuclei to taste (see Burmudez-Rattoni, 2004).
In humans an fMRI study by Small and colleagues (2003) showed that although
the amygdala and mid-insula respond to taste intensity rather than valence, the anterior
insula responds to valence regardless of intensity. In this study the left AI was
preferentially activated by unpleasant tastes. The dissociation of valence from intensity
Disgust: Sensory Affect or Primary Emotional System? 17
and of pleasant from unpleasant is consistent with the notion that separate neural
substrates underlie the pleasure and disgust systems.
Arousal that outlasts precipitating events
As discussed above the insula provides feedback to lower taste centres producing
changes in hedonic value which appear to outlast the immediate effects of illness. The
DISGUST system organizes the long-term adaptive responses of conditioned aversions
and immune alterations, thereby fulfilling Panksepp’s (1998) criterion that a basic
emotion have consequences which outlast the initiating stimuli. In humans the emotion of
disgust is accompanied by autonomic changes (Levenson, et al., 1990) and autonomic
changes tend to be longer-lasting than the sensory stimuli which trigger their production.
The human insula is also activated by self-induced disgust generated by recall and reexperience of salient personal situations (Fitzgerald, Posse, Moore, Tancer, Nathan &
Phan, 2004) indicating that disgust and its neural correlates can occur without the
presence of external stimuli.
Modification and channelling of cognitive abilities
Long-lasting behavioural plasticity is a characteristic not found in a reflexive
response such as distaste, although it is seen in both primary and secondary emotions.
While distaste is a sensory affect and may give rise to reflexive responses, responses of
the DISGUST emotional system give rise to primary emotions which may be affected by
learning. In humans the blending of primary DISGUST and complex cognitions gives
rise to secondary emotions such as moral disgust.
Even though some tastes (e.g. quinine) are intrinsically noxious giving rise to
distaste, activation of the DISGUST system usually involves learning. Furthermore a
Disgust: Sensory Affect or Primary Emotional System? 18
taste need not have negative hedonic value to produce disgust, as shown by the ease with
which CTA can be elicited to sweet tastes paired with illness. This again supports the
notion that the disgust response of humans arose not specifically as a reaction to the
hedonic properties of taste but as a reaction to cues associated with increased likelihood
of illness (see Curtis & Biran, 2001; Curtis et al., 2004). In rats CTAs may form when
taste is associated with nausea either due to gastrointestinal toxins (LiCl, nicotine etc.),
X-ray, or body rotation but not when taste is paired with shock or lactose, neither of
which gives rise to upper gastrointestinal distress (Pelchat et al., 1983; see Parker, 2003).
In humans there is a close but imperfect correlation between nausea and disgust (Rozin &
Fallon, 1987). The initial formation in an organism of a taste aversion seems to involve
gastrointestinal distress, just as the formation of a conditioned fear response to a neutral
stimulus may require pairing with shock, but once the CTA is formed aversion proceeds
without illness suggesting that the DISGUST system is activated as a learned response.
CTAs also form in one trial to a novel taste paired with bacterial antigens which produce
an immune response normally associated with illness (e.g. Pacheco-Lopez et al., 2004)
suggesting that these bacterial antigens may also produce nausea in the rat.
A number of experiments have shown that learned taste avoidance (measured in
amount drunk) can be dissociated from learned taste aversion (measured by gapes, chin
wiping etc.). In her review of this work Parker (2003) uses the term “disgust reaction” to
refer to oral gaping by which rats reject fluid infused into the mouth. She suggests that
reduced drinking from a spout measures both appetitive and consummatory responses not
necessarily involving disgust, whereas gaping or retching produced by intraoral infusion
Disgust: Sensory Affect or Primary Emotional System? 19
provides a measure of consummatory response alone. Measuring aversion by gaping and
retching in rats should therefore give an indication of activation of the DISGUST system.
Work by Parker and her colleagues shows that in rats, treatments pairing taste and
a drug that produces conditioned taste aversion (as measured by gaping during intraoral
infusion) also produce avoidance of the paired taste (as measured by voluntary drinking),
but not all treatments producing avoidance of the taste lead to conditioned aversion (see
Parker, 2003). Antinausea treatments reduce taste aversion as measured by gaping in rats,
but not taste avoidance, suggesting that nausea or malaise is necessary for the
establishment of a conditioned taste aversion. Of course conditioning is not necessary to
produce all taste aversion responses, as some inherently bad-tasting substances produce
distaste aversion which is not eliminated by antiemetics.
Innate distaste responses are found in normal and decerebrate infant mammals
including anencephalic human infants (Steiner et al., 2001). A learned response to a tasteillness pairing, however, is not a reflexive sensory affect but involves an affective
behavioural programme, i.e. the disgust reaction. A case study reported by Adolphs,
Tranel, Koenigs and Damasio (2005) illustrates this dissociation in a human patient with
bilateral damage to the insula, amygdala, hippocampus and parts of the neocortex. This
man has normal taste preference when sequentially comparing two fluids, although he
appears to have no conscious explanation for his preference. He prefers strong sucrose
solution over strong salt solution when presented sequentially but completely lacks taste
recognition of the stimuli presented separately, appearing to have no conscious
recognition of either. In other words because the brainstem gustatory areas are all intact
he shows the sensory affect, but not the full disgust component. This also suggests that at
Disgust: Sensory Affect or Primary Emotional System? 20
least in humans the disgust response is a conscious affect whereas distaste need not be
conscious.
The sensory affect-like distaste response of earlier vertebrates has been elaborated
on with the unique development of the insula in humans and the concomitant
development of subjective awareness. Thus the role of the insula is not limited to
providing an anatomical substrate for disgust. The indirect visceral pathway between
insula and amygdala which enabled the formation of CTA in rodents was replaced in
primates with a direct thalamocortical pathway allowing greater cortical integration of
sensory inputs from multiple modalities. The human insula, as described by Craig (2002,
2003, 2005) has come to play a major role underlying the distinctively human experience
of consciousness, a form of consciousness which according to Burgdorf and Panksepp
(2006) arose out of ancient forms of core consciousness supported by brain stem
structures. We are thus suggesting that the primitive emotive circuit which originally
functioned to defend the self by regulating consummatory behaviours gave rise to a
primary emotional system which facilitates evaluation of reinforcers. This is consistent
with Rozin and Fallon’s view (1987) of the elaboration of the disgust mechanism in
humans. The disgust-associated circuitry became further enriched in primates by
development of a direct thalamocortical pathway that interacts with multimodal inputs as
described by Craig (2003). In addition the unique spindle cells found in deep layers of the
cingulate cortex of humans and great apes but no other mammals, are also found in
human agranular and dysgranular AI (Nimchinsky, Gilissen, Allman, Perl, Erwin & Hof,
1999). Heimer and Van Hoesen (2006) go so far as to suggest that the right AI is not only
Disgust: Sensory Affect or Primary Emotional System? 21
crucial for emotional awareness, but “the final breeding ground for subjective feeling
states”.
Facilitated by abundant reciprocal connections to the adjacent orbitofrontal
cortex, this evaluative emotional system acquired a role in self-consciousness and
complex-decision making. Core representations of the body in the proto-self arising from
structures such as the insula (Damasio, 1999, p.156) may play a role not only in selfawareness, but also in an “as-if” loop system that allows evaluation and anticipation of
events. So the human insula rather than providing a mere module for disgust, participates
together with other areas in the instantiation of a variety of conscious feeling states.
The AI plays a role in the acquisition of the “gut feeling” developed by subjects
during the Iowa gambling task (Bechara & Damasio, 2005; see also Dunn, Dalgleish, &
Lawrence, 2006). The right AI mediates subjective awareness of heart rate timing; and
the activity and volume of AI are correlated with the accuracy of this awareness
(Critchley et al., 2004). The right insula is also activated by anticipation of emotionally
aversive visual stimuli (Simmons, Mathews, Stein, & Paulus, 2004). In individuals who
practice meditation, the number of years of practice correlates with the volume of the
right AI (Lazar, Kerr, Wasserman, Gray, Greved, Treadway et al., 2005). Probably
related to activation by disgusting stimuli, right AI is also somewhat activated by
unpleasant moral scenarios (Moll, Oliveira-Souza, Eslinger, Bramati, Mourão-Miranda,
Andreiuolo, et al., 2002).
Many behaviours integrating higher cognitive processing with “gut level” feelings
also activate AI, especially on the right. For example right AI activation is correlated with
the degree of risk during decision-making as well as the degree of harm avoidance and
Disgust: Sensory Affect or Primary Emotional System? 22
neuroticism in individuals (Paulus, Rogalsky, Simmons, Feinstein, & Stein 2003). Unfair
offers of monetary reward which the authors suggested to be a form of emotion-based
disgust activate AI more strongly on the right (Sanfey, Rilling, Aronson, Nystrom, &
Cohen, 2003). While the right AI seems to play a special role in other subjective states,
studies using unpleasant tastes, odors, or evaluating disgust often report more
involvement on the left (e.g. Calder et al., 2000; Hennenlotter et al., 2004; Royet et al.,
2003; Schienle et al., 2005; Small et al., 2003; Wicker et al., 2003).
Goldman and Sripada (2005) have pointed out that the reading of basic emotions
in the faces of others may have unique survival value involving specialized neural
programs which attribute a state in another based on simulation of that state in oneself.
They note this may be accomplished by a reverse simulation which would require an as-if
loop if it were not to depend on actual facial feedback, or alternatively observation of the
target’s face might trigger activation of the same neural substrate in the observer. The
somatic marker hypothesis of Damasio proposes the role of the insula is primarily to
provide sensory representation of the bodily state as part of an as-if mechanism. On the
other hand Gallese, Keysers and Rizzolatti (2004) propose the key activation of the insula
in social cognition is as a viscero-motor centre which simulates the activity of the other
person in a manner similar to the “mirror” neurons which they previously found in
monkeys. Hence Wicker and colleagues (2003) were able to show, using the same
subjects, that activity in left AI subserves both the experience of disgust and its
recognition in others. In the same manner both the bodily state of pain as well as
anticipation of pain in a loved one activated the right AI, and individual empathy scores
correlated with the level of activity in the right AI while the loved one was experiencing
Disgust: Sensory Affect or Primary Emotional System? 23
pain (Singer, Seymour, O'Doherty, Kaube, Dolan, & Frith, 2004). A recent follow up
study showed that the AI activity in response to pain in another person was modulated by
the perceived fairness of that person (Singer, Seymour, O'Doherty, Stephan, Dolan, &
Frith, 2006). Perhaps the two sides of the insula have become specialized for divergent
roles in self-awareness, with the left side playing a greater role in signalling and
perceiving danger to the internal milieu and the right in processing other forms of self
and other awareness.
Conclusion
We have argued here the case that disgust is a primary emotional system, with
roots deep back in our pre-mammalian ancestors. There are reasons to believe it might
have indeed been the first such system, arising out of links between the immune system
and the central nervous system, indeed possibly being the origin of the system of Neural
Darwinism. In a companion paper (Toronchuk & Ellis, forthcoming) we propose a
complete set of primary emotional systems, including DISGUST. Completion of a list of
such primary emotions, developing from the work of Darwin, Ekman, Panksepp, and
many others, is a key step in identifying the psychological factors guiding development
of higher level brain functioning. This in turn has implications for psychology, learning,
economics, and many other aspects of human behaviour. It is for this reason that we
believe that the kinds of argument presented in this paper are important.
Some have argued that the concept of basic emotions is not useful (e.g. Ortony &
Turner, 1990; Rolls 2005b, pp.31-32), proposing in essence that there is a onedimensional basic evaluation system guiding brain development, with the (apparent)
Disgust: Sensory Affect or Primary Emotional System? 24
basic emotions evolving out of this system in a systematic way (but not themselves being
genetically determined). We believe rather that a multi-dimensional genetically
determined system as envisaged by Panksepp (1998) and ourselves (Ellis & Toronchuk,
2005) is needed because a 1-dimensional system simply does not have the ability to
structure a brain in the developmental time available, and indeed even if slower were
acceptable, probably can't do the job with sufficient refinement and accuracy to meet the
brain's developmental and functional needs in any case. Thus we see basic emotions
playing a key role in brain evolution and development (as discussed in Ellis &
Toronchuk, 2005). If this is correct, in understanding brain development it is crucial to
determine which emotional systems are primary (that is, mainly genetically determined)
and which are secondary (that is, determined mainly by developmental processes as the
mind interacts with the local social environment). Investigating this may generate useful
future research on evolutionary and developmental processes.
We see two further significant reasons to discuss which emotions should be
considered basic. Firstly, focusing attention on the biological functions of these systems
in the evolutionary past has led psychology to a greater awareness of biological
complexities of human emotions. This has led and will continue to lead to new treatments
and diagnostic techniques for psychiatric disorders. Secondly because of the complex
interaction of genetic and environmental components in the ontogeny of basic emotions,
the consideration of developmental mechanisms may lead to new ideas on the promotion
of healthy emotional development in human children.
Disgust: Sensory Affect or Primary Emotional System? 25
FOOTNOTES
1
We follow Panksepp in the use of capitals to denote an emotional organising system
rather than an emotion per se.
Disgust: Sensory Affect or Primary Emotional System? 26
REFERENCES
Adolphs, R., Tranel, D., Koenigs, M., &, Damasio, A. R.(2005). Preferring one taste over
another without recognizing either. Nature Neuroscience, 8, 860-861.
Alvarez-Borda, B., Ramirez-Amaya, V., Perez-Montfort, R., & Bermudez-Rattoni,
F.(1995). Enhancement of antibody production by a learning paradigm.
Neurobiology of Learning & Memory, 64 (2), 103-105.
de Araujo, I.E.T., Rolls, E.T., Kringelbach, M.L., McGlone, F., & Phillips, N. (2003).
Taste-olfactory convergence and the representation of the pleasantness of flavour,
in the human brain. European Journal of Neuroscience, 18, 2059-2068.
Bechara, A., & Damasio, A.(2005). The somatic marker hypothesis: A neural theory of
economic decision. Games and Economic Behavior 52, 336–372.
Berman, D.E., Hazvi, S., Neduva, V., & Dudai, Y. (2000). The role of identified
neurotransmitter systems in the response of insular cortex to unfamiliar taste:
activation of ERK1–2 and formation of a memory trace. The Journal of
Neuroscience, 20, 7017–7023.
Bermudez-Rattoni, F.(2004). Molecular mechanisms of taste recognition memory, Nature
Reviews: Neuroscience, 5, 209-217.
Bermudez-Rattoni, F., Grijalva, C.V., Kiefer, S.W., &. Garcia, J. (1986). Flavor-illness
aversions: the role of the amygdala in the acquisition of taste-potentiated odor
aversions. Physiological Behavior, 384, 503-508.
Bernstein, I.L. (1999). Taste aversion learning: a contemporary perspective. Nutrition,
15, 229-234.
Disgust: Sensory Affect or Primary Emotional System? 27
Burgdorf, J., & Panksepp, J. P.(2006). The neurobiology of positive emotions.
Neuroscience and Biobehavioral Reviews, 30, 173–187.
Calder, A. J., Keane, J., Manes, F., Antoun, N., & Young, A.W.(2000). Impaired
recognition and experience of disgust following brain injury. Nature
Neuroscience, 3, 1077-1078.
Carew, T. J., & Sahley, C. L.(1986). Invertebrate learning and memory: from behaviour
to molecules. Annual Review of Neuroscience, 9, 435–-487.
Cechetto, D.F., &. Saper, C.B. (1987) Evidence for a viscerotopic sensory representation
in the cortex and thalamus in the rat. Journal of Comparative Neurology, 262, 2745.
Craig, A. D. (2002). How do you feel? Interoception: the sense of the physiological
condition of the body. Nature Reviews: Neuroscience, 3, 655-666.
Craig, A. D. (2003). Interoception: the sense of the physiological condition of the body.
Current Opinion in Neurobiology, 13, 500–505.
Craig, A.D. (2005). Forebrain emotional asymmetry: a neuroanatomical basis? Trends in
Cognitive Sciences, 9, 566-571.
Critchley, H. D., & Rolls, E.T.(1996). Olfactory neural responses in the primate
orbitofrontal cortex: Analysis in an olfactory discrimination task. Journal of
Neurophysiology, 75, 1659-1672.
Critchley, H .D., Rotshtein, P., Nagai, Y., O'Doherty, J., Mathias, C. J., & Dolan, R.
J.(2005). Activity in the human brain predicting differential heart rate responses
to emotional facial expressions. NeuroImage, 24, 751-762.
Disgust: Sensory Affect or Primary Emotional System? 28
Critchley, H. D., Wiens, S., Rotshtein, P., Öhman, A., & Dolan, R. J. (2004). Neural
systems supporting interoceptive awareness. Nature Neuroscience, 7, 189-195.
Curtis, V. A., & Biran, A.(2001). Dirt, disgust and disease: is hygiene in our genes?
Perspectives in Biology and Medicine, 44, 17–31.
Curtis, V., Aunger, R., & Rabie, T.(2004). Evidence that disgust evolved to protect from
risk of disease. Proceedings of the Royal Society of London. Series B. Biological
Sciences, 271, 131-133.
Damasio, A.R. (1999). The feeling of what happens: body and emotion in the making of
consciousness. New York, NY: Harcourt.
Damasio, A. R., Grabowski, T. J., Bechara, A., Damasio, H., Ponto, L. L., Parvizi, J., et
al. (2000). Subcortical and cortical brain activity during the feeling of selfgenerated emotions. Nature Neuroscience, 3, 1049-1056.
Domjan, M.(2005). Pavlovian conditioning: a functional perspective. Annual Review of
Psychology, 56, 179–206.
Dunn, B. D., Dalgleish, T., & Lawrence, A. D.(2006). The somatic marker hypothesis: A
critical evaluation. Neuroscience & Biobehavioral Reviews, 30, 239-271.
Egan, G., Silk, T., Zamarripa, F., Williams, J., Federico, P., Cunnington, R. et al. (2003).
Neural correlates of the emergence of consciousness of thirst. Proceedings of the
National Academy of Science, U.S.A., 100, 15241-15246.
Ekman, P., & Friesen, W. V.(1986). A new pan-cultural facial expression of emotion.
Motivation and Emotion, 10, 159-168.
Ellis, G. F.R., & Toronchuk, J. A.(2005). Neural development: Affective and immune
system influences. In N. Newton, & R. Ellis (Eds.), Consciousness and emotion:
Disgust: Sensory Affect or Primary Emotional System? 29
Agency, conscious choice and selective perception (pp.81-119). Philadelphia, PA:
John Benjamins.
Fitzgerald, D. A., Posse, S., Moore, G. J., Tancer, M. E., Nathan, P. J., & Phan,
K.L.(2004). Neural correlates of internally-generated disgust via autobiographical
recall: a functional magnetic resonance imaging investigation. Neuroscience
Letters, 370, 91-96.
Flynn, F. G., Benson, D. F., & Ardila, A.(1999). Anatomy of the insula--functional and
clinical correlates. Aphasiology, 13, 55-78.
Galati, D., Scherer, K.R., & Ricci-Bitti, P.E. (1997) Voluntary facial expression of
emotion: comparing congenitally blind with normally sighted encoders. Journal
of Personality and Social Psychology, 73, 1363-1379.
Gallese, V., Keysers, C., & Rizzolatti, G. (2004).A unifying view of the basis of social
cognition. Trends in Cognitive Science 8, 396-404.
Garcia, J., Hankins, W. G., & Rusiniak K. W.(1974). Behavioral regulation of the milieu
interne in man and rat. Science, 185, 824-831.
Garcia, J., Quick, D. F., & White, B.(1984). Conditioning disgust and fear from mollusk
to monkey. In D. Alkon, & J. Farley, Primary neural substrates of learning and
behavioral change (pp. 47-61).Cambridge University Press.
Goldman, A. I. & Sripada, C. S.(2005). Simulationist models of face-based emotion
recognition. Cognition, 94, 193-213.
Gottfried, J. A., & Zald, D. H.(2005). On the scent of human olfactory orbitofrontal
cortex: meta-analysis and comparison to non-primates. Brain Research Reviews,
50, 287-304.
Disgust: Sensory Affect or Primary Emotional System? 30
Heimer, L.,& Van Hoesen, G. W. (2006). The limbic lobe and its output channels:
Implications for emotional functions and adaptive behaviour. Neuroscience and
Biobehavioral Reviews 30, 126-147.
Hennenlotter, A., Schroeder, U., Erhard, P., Haslinger, B., Stahl, R., Weindl, A., et al.
(2004). Neural correlates associated with impaired disgust processing in presymptomatic Huntington's disease. Brain, 127, 1446-53.
Hornby, P. J. (2001). Central neurocircuitry associated with emesis. The American
Journal of Medicine, 111 Supplement 8A, 106S-112S.
Horton, J., & Ratcliffe N.A.(2001) Evolution of Immunity In I. Roitt, J. Brostoff, & D.
Male, Immunology 6th ed. Toronto, ON: Mosby.
Hosie, J.A., Gray, C.D., Russell, P. A., Scott, C., & Hunter, N.(1998). The matching of
facial expressions by deaf and hearing children and their production and
comprehension of emotion labels. Motivation and Emotion, 22, 293-313.
Kiefer, S.W., & Orr, M. R.(1992).Taste avoidance, but not aversion, learning in rats
lacking gustatory cortex. Behavioral Neuroscience, 106, 140-146.
Koh, M. T., & Bernstein, I. L.(2005). Mapping conditioned taste aversion associations
using c-Fos reveals a dynamic role for insular cortex. Behavioral Neuroscience,
1192, 388-398.
Krolak-Salmon, P., Henaff, M.-A., Isnard, J., Tallon-Baudry, C., Guenot, M., Vighetto,
A., et al.(2003). An attention modulated response to disgust in human ventral
anterior insula. Annuals of Neurology, 53, 446-453.
Disgust: Sensory Affect or Primary Emotional System? 31
Lane, R. D., Reiman, E. M., Ahern, G. L., Schwartz, G. E., & Davidson, R. J. (1997).
Neuroanatomical correlates of happiness, sadness, and disgust. The American
Journal of Psychiatry, 154, 926-933.
Lasiter, P. S., Deems, D.A., Oetting, R. L., & Garcia. J. (1985). Taste discriminations in
rats lacking anterior insular gustatory neocortex. Physiological Behavior, 352,
277-285.
Lazar, S. W., Kerr, C. E., Wasserman, R. H., Gray, J. R., Greved, G. N., Treadway, M.
T., et al. (2005). Meditation experience is associated with increased cortical
thickness NeuroReport, 16, 1893-1897.
Lawes, I.N. (1990). The origin of the vomiting response: a neuroanatomical hypothesis.
Canadian Journal of Physiological Pharmacology, 682, 254-259.
Lawrence, A. D., & Calder, A. J.(2004). Homologizing human emotions. In D. Evans &
P. Cruse (Eds.), Emotion, evolution and rationality (pp. 15-47). Oxford University
Press.
Levenson, R. W., Ekman, P., & Friesen, W. V.(1990). Voluntary facial action generates
emotion-specific autonomic nervous system activity. Psychophysiology, 27, 363384.
Liotti, M., Mayberg, H. S., Brannan, S. K., McGinnis, S., Jerabek, P., & Fox, P. T.
(2000). Differential limbic-cortical correlates of sadness and anxiety in healthy
subjects: implications for affective disorders. Biological Psychiatry, 48, 30-42.
Lundy, R. F., & Norgren, R. (2004).Activity in the hypothalamus, amygdala, and cortex
generates bilateral and convergent modulation of pontine gustatory neurons.
Journal of Neurophysiology, 91, 1143-1157.
Disgust: Sensory Affect or Primary Emotional System? 32
Mesulam, M.-M., & Mufson, E. J.(1982). Insula of the old world monkey. III: Efferent
cortical output and comments on function. Journal of Comparative Neurology,
212, 38-52.
Miller, S.B. (2004) Disgust: The gatekeeper emotion. Hillsdale, NJ.: The Atlantic Press.
Miller, W.I. (1997). The anatomy of disgust. Cambridge, MA: Harvard University Press.
Miranda, M. I., Ferreira, G., Ramirez-Lugo, L., & Bermúdez-Rattoni, F.(2002).
Glutamatergic activity in the amygdala signals visceral input during taste memory
formation. Proceeding of the National Academy of Science, USA, 99, 11417–
11422.
Morris, J.S., Friston, K.J., Büchel, C., Frith, C.D., Young, A.W., Calder, A.J., et al.
(1998). A neuromodulatory role for the human amygdala in processing emotional
facial expressions. Brain, 121, 47-57.
Moll, J., Oliveira-Souza, R., Eslinger, P. J., Bramati, I. E., Mourão-Miranda, J.,
Andreiuolo, P.A., et al.(2002). The neural correlates of moral sensitivity: a
functional magnetic resonance imaging investigation of basic and moral emotions.
The Journal of Neuroscience, 22, 2730-2736.
Nimchinsky, E. A., Gilissen, E., Allman, J. M., Perl, D. P., Erwin, J. M., & Hof, P.
R.(1999). A neuronal morphologic type unique to humans and great apes.
Proceeding of the National Academy of Sciences, USA, 96, 5268-5273.
Mufson, E. J., Mesulam, M. M., & Pandya, D. N.(1981). Insular interconnections with
the amygdala in the Rhesus monkey. Neuroscience, 6, 1231-1248.
Disgust: Sensory Affect or Primary Emotional System? 33
O’Doherty J., Rolls, E.T., Francis, S., Bowtell, R., & McGlone, F. (2001). The
representation of pleasant and aversive taste in the human brain. Journal of
Neurophysiology, 85, 1315–21.
Öhman, A., & Mineka, S. (2001). Fears, phobias, and preparedness: toward an evolved
module of fear and fear learning. Psychological Review, 108, 483-522.
Ortony, A., & Turner, T.J.(1990). What's basic about basic emotions? Psychological
Review, 97, 315-331.
Pacheco-López, G., Niemi, M.-B., Kou, W., Härting, M., Del Rey, A., Besedovsky, H.
O., & Schedlowski, M.(2004). Behavioral endocrine immune conditioned
response is induced by taste and superantigen pairing. Neuroscience, 129, 555562.
Panksepp, J. (1998). Affective neuroscience: The foundations of human and animal
emotions. London, UK: Oxford University Press.
Panksepp, J. (2000). Emotions as natural kinds within the mammalian brain. In M. Lewis
& J.M. Haviland-Jones, (Eds.), The handbook of emotions, 2nd ed. (pp.137-156).
New York, NY: Guilford Press.
Panksepp, J. (2005). Affective consciousness: core emotional feelings in animals and
humans. Consciousness and Cognition, 14, 30–80.
Parker, L. A. (2003). Taste avoidance and taste aversion: evidence for two different
processes. Learning & Behavior, 312, 165-172.
Paulus, M. P., Rogalsky, C., Simmons, A., Feinstein, J. S, & Stein, M. B.(2003).
Increased activation in the right insula during risk-taking decision making is
related to harm avoidance and neuroticism. NeuroImage, 19, 1439–1448.
Disgust: Sensory Affect or Primary Emotional System? 34
Pelchat, M. L., Grill, H. J., Rozin, P., & Jacobs, J.(1983). Quality of acquired responses
to tastes by Rattus norvegicus depends on types of associated discomfort. Journal
of Comparative Psychology, 97, 140-153.
Phillips, M. L., Young, A. W., Senior, C., Brammer, M., Andrew, C., Calder, A. J., et al.
(1997). A specific neural substrate for perceiving facial expressions of disgust.
Nature, 389, 495-498.
Ramirez-Amaya, V., Alvarez-Borda, B., & Bermudez-Rattoni, F.(1998). Differential
effects of NMDA-induced lesions into the insular cortex and amygdala on the
acquisition and evocation of conditioned immunosuppression. Brain, Behavior,
and Immunity, 12, 149-160.
Ramirez-Amaya, V., & Bermudez-Rattoni, F.(1999). Conditioned enhancement of
antibody production is disrupted by insular cortex and amygdala but not
hippocampal lesions. Brain, Behavior, and Immunity, 13, 46-60.
Ritz, T., Thons, M., Fahrenkrug, S., & Dahme, B.(2005) Airways, respiration, and
respiratory sinus arrhythmia during picture viewing. Psychophysiology, 42, 568578.
Rolls, E. T.(1989). Information processing in the taste system of primates. Journal of
Experimental Biology, 146, 141-164.
Rolls, E. T.(2005a). Taste, olfactory, and food texture processing in the brain, and the
control of food intake. Physiology & Behavior, 85, 45-56.
Rolls, E. T.(2005b). Emotions explained. (Oxford University Press, Oxford).
Disgust: Sensory Affect or Primary Emotional System? 35
Royet, J.-P., Plailly, J., Delon-Martin, C., Kareken, D. A., & Segebarth, C.(2003). fMRI
of emotional responses to odors: Influence of hedonic valence and judgment,
handedness, and gender. NeuroImage, 20, 713–728.
Rozin, P., & Fallon, A. E.(1987). A perspective on disgust. Psychological Review, 94,
23-41.
Rozin, P., Haidt, J., & McCauley, C. R.(1999). Disgust: the body and soul emotion .In T.
Dalgleish & M. J.. Power, (Eds.),The handbook of cognition and emotion, 2nd ed.
(pp. 429-445). Chichester, UK: John Wiley.
Rozin, P., & Kalat, J. W.(1971). Specific hungers and poison avoidance as adaptive
specializations of learning. Psychological Review, 78, 459-486.
Rubio-Godoy, M., Aunger, R., & Curtis, V.(2007). Serotonin—a link between disgust
and immunity? Medical Hypotheses, 68, 61-66.
Sanfey, A. G., Rilling, J. K., Aronson, J. A., Nystrom, L. E., & Cohen, J. D. (2003). The
neural basis of economic decision-making in the ultimatum game. Science, 300,
1755-1758.
Saper, C.B. (2002). The central autonomic nervous system: conscious visceral perception
and autonomic pattern generation. Annual Review of Neuroscience, 25, 433-469.
Schafer, A., Schienle, A., & Vaitl, D.(2005). Stimulus type and design influence
hemodynamic responses towards visual disgust and fear elicitors. International
Journal of Psychophysiology, 57, 53-59.
Schienle, A., Schafer, A., Stark, R., Walter, B., & Vaitl, D.(2005). Relationship between
disgust sensitivity, trait anxiety and brain activity during disgust induction.
Neuropsychobiology, 51, 86-92.
Disgust: Sensory Affect or Primary Emotional System? 36
Schienle, A., Stark, R., Walter, B., Blecker, C., Ott, U., Kirsch P., et al.(2002). The insula
is not specifically involved in disgust processing: an fMRI study. Neuroreport,
13, 2023-2026.
Shapira, N. A., Liu, Y., He, A. G., Bradley, M. M., Lessig, M. C., James, G. A., et
al.(2003). Brain activation by disgust-inducing pictures in obsessive-compulsive
disorder. Biological Psychiatry, 54, 751-756.
Simmons, A., Mathews, S. C., Stein, M. B., & Paulus, M. P.(2004). Anticipation of
emotionally aversive visual stimuli activates right insula. NeuroReport, 15, 22612265.
Singer, T., Seymour, B., O'Doherty, J., Kaube, H., Dolan, R. J., & Frith, C. D.(2004).
Empathy for pain involves the affective but not sensory components of
pain.
Science, 303, 1157-1162.
Singer, T., Seymour, B., O'Doherty, J. P., Stephan, K. E., Dolan, R. J., & Frith, C. D.
(2006). Empathic neural responses are modulated by the perceived fairness of
others. Nature, 439, 466-469.
Spector, A. C. (2000), Linking gustatory neurobiology to behavior in vertebrates.
Neuroscience and Biobehavioral Reviews, 24, 391–416.
Sprengelmeyer, R., Young, A. W., Calder, A. J., Karnat, A., Lange, H., Hömberg, V., et
al. (1996). Loss of disgust. perception of faces and emotions in Huntington's
disease. Brain: a Journal of Neurology, 119, 1647-1665.
Sprengelmeyer, R., Young, A. W., Mahn, K., Schroeder, U., Woitalla, D., Büttner, T., et
al.(2003). Facial expression recognition in people with medicated and
unmedicated Parkinson's disease. Neuropsychologia, 41, 1047-1057.
Disgust: Sensory Affect or Primary Emotional System? 37
Sprengelmeyer, R., Young, A. W., Pundt, I., Sprengelmeyer, A., Calder, A. J., Berrios,
G., et al. (1997). Disgust implicated in obsessive-compulsive disorder.
Proceedings of the Royal Society of London. Series B. Biological Sciences, 264,
1767-1773.
Small, D. M., Gregory, M. D., Mak, Y. E., Gitelman, D., Mesulam, M. M., & Parrish,
T.(2003). Dissociation of neural representation of intensity and affective valuation
in human gustation. Neuron, 39, 701-711.
Small, D. M. Zarotte, R. J., Dagher, A., Evans, A. C., & Jones-Gotman, M.(2001).
Changes in brain activity related to eating chocolate: from pleasure to aversion.
Brain, 124, 1720-1733.
Stark, R., Walter, B., Schienle, A., & Vaitl, D.(2005). Psychophysiological correlates of
disgust and disgust sensitivity. Journal of Psychophysiology, 19, 50-60.
Steiner, J. E., Glaser, D., Hawilo, M. E., & Berridge, K. C.(2001). Comparative
expression of hedonic impact: Affective reactions to taste by human infants and
other primates. Neuroscience and Biobehavioral Reviews, 25, 53-74.
Stevenson, R.J., & Repacholi, B.M.(2005). Does the source of an interpersonal odour
affect disgust? a disease risk model and its alternatives. European Journal of
Social Psychology, 35, 375–401.
Stoléru, S., Grégoire, M.-C., Gérard, D., Decety, J., Lafarge, E., Cinotti, L., et al.(1999).
Neuroanatomical correlates of visually evoked sexual arousal in human males.
Archives of Sexual Behavior, 28, 1-21.
Disgust: Sensory Affect or Primary Emotional System? 38
Sugai, R., Shiga, S., Azami, S., Watanabe, T., Sadamoto, H., Fujito, Y., et al.(2006).
Taste discrimination in conditioned taste aversion of the pond snail Lymnaea
stagnalis. The Journal of Experimental Biology 209, 826-833.
Tataranni, P. A., Gautier, J. F., Chen, K, Uecker, P. A., Bandy, D., Salbe, A. D., et
al.(1999). Neuroanatomical correlates of hunger and satiation in humans using
positron emission tomography. Proceedings of the National Academy of Sciences,
U.S.A., 96, 4569-4574.
Toronchuk, J. A. & Ellis, G.F.R.(in preparation). Affective neuronal Darwinism: the
nature of the primary emotional systems.
Wicker, B., Keysers, C., Plailly, J., Royet, J. P., Gallese, V., & Rizzolatti, G.(2003). Both
of us disgusted in my insula: The common neural basis of seeing and feeling
disgust. Neuron, 40, 655-664.
Wolf, K., Mass, R., Ingenbleek, T., Kiefer, F., Naber, D., & Wiedemann, K.(2005). The
facial pattern of disgust, appetence, excited joy and relaxed joy: an improved
facial EMG study. Scandinavian Journal of Psychology, 46, 403-409.
Yasui, Y., Breder, C. D., Saper, C. B., & Cechetto, D. F.(1991). Autonomic responses
and efferent pathways from the insular cortex in the rat. Journal of Comparative
Neurology, 303, 355-374.
Zhang, Y., Lu, H., & Bargmann, C.I.(2005). Pathogenic bacteria induce aversive
olfactory learning in Caenorhabditis elegans. Nature, 438, 179-184.
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