Disgust: Sensory Affect or Primary Emotional System?

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Disgust: Sensory Affect or Primary Emo
tional System?


1



Disgust:
S
ensory
A
ffect or
P
rimary
E
motional
S
ystem?

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





Ru
nning 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


Disgust: Sensory Affect or Primary Emo
tional System?


2




Abstract


W
e 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 evaluatio
n 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 Emo
tional System?


3

Introduction


In
this
paper we
present arguments

for the inclusion of
DISGUST

1

as a primary
emotional system
, to be included in the list o
f 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 phyl
ogeny
of neural

pathways.
Using
his
differentiation
between sensory

affect and primary emotional system, we

wish

to

argu
e
that

the

complex, action
-
oriented affective response of

the DISGUST
system should be
distinguished
from the sensory affect of

distast
e

.
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) mod
ulation

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 perceptio
n

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
belong
s
to the latter category and

is a phylogenetic development
arising from

mechanisms which orig
inally functioned to
prevent disease
.

We supp
ort this
claim below by arguing
in t
u
r
n

for its
p
hylogenetically ancient origins,
a
ctivation by
diverse sensory modalities
,
a
bility to organize diverse behaviours,
d
istinct neural

Disgust: Sensory Affect or Primary Emo
tional System?


4

circuitry,
ability to produce
c
hanges in hedonic value,

a
rousal which outlasts precipitating
events,
and m
odification and cha
nnelling of cognitive abilities



P
hylogenetically ancient origins



While psychologists have long
agree
d

in principle
with the idea that emotions
have evolutiona
ry origins
and

facilitate

adaptive actions, m
ost 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 appro
ach 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 b
asic emotion referred to in humans as
disgust

evolved from the
reflexive
distaste

response

of vertebrate ancestors
,

which in turn arose from primitive
c
hemosensory 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 al
l organisms,

no matter how simple, defend their
bodies against other
s
.
T
he 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 Emo
tional System?


5

Hankins, & Rusiniak,

1974;
Garcia, Qu
ick
,

&

White,
1984
, p. 49)
.

All
organisms

must
protect
themselves not only from external predators but also from
invasive
micro
-
organisms 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 d
anger to the internal milieu has been
signalled

by

chemosensory

detection mechanisms found in all multicellu
lar 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, & Barg
mann,
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

conditi
oned taste aversion to

either sucrose or ca
rrot 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 Emo
tional System?


6


Rozin

and his colleagues

have
suggest
ed

the phylogenetic origin of disgust

lies

in

the

distaste
/oral rejection

response
of animals

to bad tasting food (Rozin & Fallon 1987;
Rozin, Haidt, & McCau
ley, 1999).

They

hold

the
specifically human
emotion of disgust
d
iffers

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 w
ould include interpersonal and socio
-
moral disgust. More recently

Curtis and Biran (2001)
have
argue
d

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 th
e

disease model
(
Stevenson

& Repacholi
,

2005).
Rubi
o
-
Godoy, Aunger and Curtis (2007
) further

suggest
disgust is a neural system “evolved to detect reliable signals co
-
occurring with disease
-
causing infectious agents, which stimulates avoidance responses and/or other behav
iours
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

chemorecepto
rs

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 Emo
tional System?


7

thereafter
most prominent cue for
aversion responses
, other
sensations

can also be


effect
ive

triggers.
In humans
taste,
olfact
ory
, audit
ory
, tactile and visual cues
are all
capable of e
licit
ing

disgust (Cu
r
tis & 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 s
eeds 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
17
th

century

along with the aesthetic notion of “good taste”
, its

etymological
origin

has likely

b
ias
ed

English
-
speaking
researchers
to
focu
s

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 (G
arcia 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, spi
ders and angry faces

Disgust: Sensory Affect or Primary Emo
tional System?


8

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 mode
rn 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 argumen
t 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 od
our 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
divers
e behaviours


Responses of the
DISGUST
system
can
involve flexible voluntary components
,

thereby
satisfying

another
of
the criteria for

basic emotional system
s

(Pan
k
sepp, 1998,
p.4
9
).

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 s
niffing and
manipulation often followed by breaking and squashing the item, then dropping or

Disgust: Sensory Affect or Primary Emo
tional System?


9

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
i
mmune an
d 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 inte
rferon
-
γ) and
corticosterone (
Pacheco
-
L
ó
pez, Niemi, Kou, H
ä
rting,
Del Rey
,

Besedovsky
,

et al.
,
2004; also
Alvarez
-
Borda, Ramirez
-
Amaya, Perez
-
Montfort,
& Bermudez
-
Rattoni, F.
1995; Ramirez
-
Amaya & Burmudez
-
Rattoni,

1999). This
lend
s

credence to
Curtis’
disease th
eory
,

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

organ
isms

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
dr
i
nk from a tube protruding from a nose cone covered with
filter paper impregnated with
initially neutral
odour
s. 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 present
ed with
the conditioned odour
. Garcia
observed some of these

rats claw out
the
filter paper containing th
is

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 a
lso 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 Emo
tional System?


10

conductance (
Stark, W
alter,
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 voluntari
ly 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 i
s
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 fac
ial 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

t
he 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 exist
ence across species of common neural structures involved in triggering
disgust reactions

suggest
s

a unified affective system with ancient origins

which has
undergone recent elaboration

in humans
.

Both t
he
human
disgust response
and

conditi
oned taste avers
ions in animals depend

on allocortical regions of the insula
consistent with
the
suggestion that primary emotions
aris
e

from emotional operating
systems concentrated in subneocortical, limbic regions of the brain

(Panksepp, 2005).


Disgust: Sensory Affect or Primary Emo
tional System?


11


In mammals r
eflexive vom
iting 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

cent
re


that may be
activated by electrical stimula
tion
,

suggesting that emesis, like feeding, is under multiple
levels of neural control (Lawes, 1990).

. C
audal NTS
receives

visceral and immune
system input from the vagus (X
th
) nerve

and

input

regarding blood
-
borne substances
from area postrema
,

while t
h
e rostral NTS
receives taste input
from cranial nerves VII,
IX and X.

T
aste 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
;
Spe
ctor, 2000).

Some differences between primates and other
mammals are evident in the inputs to the insula
which Craig (2002, 200
5
) argues
allow
the development of a greater degree of self
-
awareness

in primates
.

In
rodents both
taste

and visceral
input is re
layed
via the pons to the thalamus and then
to the insula
(see
Saper, 2002).

V
isceral input
reaches

the
amygdala

via the pons
(
see
Bermudez
-
Rattoni,
2004)
.
F
ormation of a CTA

in rats

requires both
the
anterior
insula

(AI)

and
the
amygdala

to be intact
(L
asiter
,

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 low
er levels of the brainstem,
while
the DISGUST

programme requir
es

subneocortical limbic structures
.

The
insula
appears to be
required for rodents
to
recognize the taste as novel

(
Berman, Hazvi, N
e
duva, & Duda
i
,
2000)
,

while
the
amygdala

signal
s

the
aversive

visceral
components

of the
nausea/illness (
Miranda,
Ferreira, Ramirez
-
Lugo
,

&

Bermudez
-
Rattoni
,

2002).

L
esions in the insula not only

Disgust: Sensory Affect or Primary Emo
tional System?


12

disrupt acquisition and evocation of
CTA
, but also of immune enhancement or
suppression conditioned by either taste or ol
factory 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

t
he amygdala appears to
receive bot
h taste and visceral input from the insula

(Mesulam & Mufson, 1982
; Mufson,
Mesulam
,

& P
an
dya, 1981
),
rather than through subcortical connections from

NTS

as in
rodents

(see Rolls, 1989).
Craig (2002, 200
5
) 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 cell
s
)
,
dysgranular

and
granular
.

The
anterior insula
,
consisting
of
agranular and

the anterior portion of the
dysgranular

regions,
developed
phylogenetically as a cent
re

for processing
exteroceptive
chemosensory
input
.
More
posterior

d
ysgranular and granular regions act as visceral sensory cortex

(Saper, 2002).
Although the cytoarchite
cture 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 rich
er

interconnections

to
orbitofrontal cortex.


The
prima
te
agranular
AI
is
relatively undifferentiated allocortex (rather than
neo
cortex
)

containing
two
or

t
hree layers
which are
continuous with agranular
orbitofrontal cor
t
ex
(
see

Flynn et al., 1999
; Gottfried & Zald, 2005
)
.
This region, like the
adjacent orbit
ofrontal 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 Emo
tional System?


13

the orbitofrontal cortex (Gottfried & Zald, 2005), although the agranular
AI
is also
activa
ted by

olfaction and

taste (
de Araujo, Rolls, Kringelbach, McGlone
,

& Phillips,

2003
).
Dors
al 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
m
ammalian
isocortex (neocortex)
.
In rodents the taste area is found here
(
Cechetto &
Saper,
1987
)

and electrical stimulation of dysgranular insula produce
s
gastric motility (Yasui, Breder, Saper
,

& Cechetto, 1991).
Monkey

neurons in
AI
respond
to taste
,

olf
action, vision, texture
or

temperature of food (
see

Rolls,
2005
a
).



Human

neuroimaging studies show
th
at

AI

is

involved

in coding

taste

sensation
,
olfaction,
the reward value of taste (
Royet, Plailly, Delon
-
Martin, Kareken, & Segebarth,
2003;

Small, Grego
ry, 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 aw
areness of:
thirst (
Egan, Silk
,

Zamarripa,
Williams, Federico,
Cunnington et

al.
,

2003), hunger (Tataranni, Gautier, Chen,

Uecker, Bandy,

Salb
e

et a
l.,

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 c
audal 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, t
emperature,

hunger, thirst
,

etc
.

(
see
Craig, 2002; 2003
)
.



Disgust: Sensory Affect or Primary Emo
tional 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
s
timulation of insula in human
s invokes unpleas
ant 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 “dif
ficult 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, Schr
oeder, 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, Plail
ly, 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
,

19
97;

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 DISG
UST

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 Emo
tional 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
(
Phi
l
lips et al., 1997;
Schafer,
Schienle, & Vaitl,

2005
;
Schienle et al
.,

2002
;
S
c
hienle, 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
,

H
ö
mberg et al., 1996; Sprengelmeyer, Young, Mahn, Schroeder, Woitalla,
B
ü
ttner et al., 2003; Sprengelme
yer, 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 function
s of
the human insula will be considered below.

Changes in hedonic value


The DISGUST system is able to produce c
hanges in the hedonic value of tastes
consistent with

the
third criterion

outlined
above

(
Panksepp
,

199
8
,

p. 49
;

Panksepp,

2000
).

CTA

can be el
icited 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 o
ccurs 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

p
referred

taste actually
became aversive.



Disgust: Sensory Affect or Primary Emo
tional System?


16


Experiments by Kiefer
and

Orr (1992) confirm
that CTA involves changes in
hedonic value.

Lesions in
the
insula
r
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

no
t entail a palatability shift whereas the
insular
taste area

is necessary for the shift in palatability that occurs in learned taste aversions.

Furthermore e
lectrical stimulation of
insula

in anesthetised rats can modulate both
posit
ively 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 Li
Cl
,

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 t
he 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 mechani
sm 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

respond
s

to valence regardless of intensity. In th
is

study the left
AI

was
preferentially activated by unpleasant tastes.

The dissociation of valence from intensity

Disgust: Sensory Affect or Primary Emo
tional System?


17

and of pleasant from unpleasant is consistent with the notion
that
se
parate neural
substrates
underlie the pleasure and disgust systems.


Arousal
that

o
utlasts precipitating
events


As discussed above the insula provides feedback to lower taste

centre
s producing
changes in hedonic value

which appear to outlast the immediat
e 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 disg
ust generated by recall and re
-
experience 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.

M
odification and channel
ling of cognitive abilities


Long
-
lasting b
ehavioural
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 ref
lexive 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 tho
ugh some

tastes
(e.g.

quinine
)

are
intrinsically noxious
giving

rise to
distaste
,

activation of the DISGUST system usually
involve
s

learning
.
Furthermore a

Disgust: Sensory Affect or Primary Emo
tional System?


18

taste need not have negative hedonic value to produce disgust, as shown by the ease with
which CTA c
an 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, ne
ither 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 a
version

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 i
s 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 ma
y 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) use
s 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 o
r retching produced by intraoral infusion

Disgust: Sensory Affect or Primary Emo
tional 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 produce
s

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 a
voidance 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 d
istaste responses are found in
normal and

decerebrate infant mammals
including anencephalic human infants

(Steiner et al., 2001)
.
A learned response to a taste
-
illness 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 sequential
ly 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 separ
ately, 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 Emo
tional System?


20

least in humans the disgust respons
e is a conscious affect whereas distaste

need not be
conscious.



The
sensory affect
-
like
d
istaste

response of earlier vertebrates

has been elaborated
on with the unique development of the insula in humans

and the concomitant
development of subjective awar
eness
.

Thus the role of the insula is not limited to
providing an anatomical substrate for disgust.
T
he indirect visceral pathway
between

insula and

amygdala

which
enabled

the formation

of CTA

in

rodent
s

was replaced in
primates

with
a
direct thalamocortic
al pathway allow
ing

greater
cortical
integration
of
sensory inputs from
multiple
modalities
.
T
he
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 r
egulating consummatory behaviours gave rise to a
prima
ry

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
-
a
ssociated circ
uitry became
further
e
nriched

in primates

by
development of a
direct
thalamocortical pathway that
interact
s

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 Emo
tional System?


21

crucial for emotional awarene
ss, but “the final breeding ground for subjective feeling
states”.


F
acilitated by
abundant reciprocal
connections to the adjacent orbitofrontal
cortex
,

this evaluative emotional system
acquir
ed
a role

in self
-
cons
c
iousness

and
complex
-
decision making
.

C
or
e 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 self
-
awareness, 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 Io
wa gambling task (
Bechara & Damasio, 2005
; see also Dunn, Dalgleish,

&

Lawrence, 2006). T
he 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 (Si
mmons
, 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
disgust
ing stimuli
,
right AI
is also
somewhat activated
by
unpleasant moral scenarios (
Moll, Oliveira
-
Souza, Eslinger, Bramati, Mourão
-
Miranda,
Andreiuolo,

et al.
, 2002
).


M
any 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 Emo
tional 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, Rilli
ng, Arons
on, 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; Hennenlotte
r 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 alternativ
ely 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 bod
ily

state

as part
of an
a
s
-
if mechanism. On the
other hand

Gallese, Keysers and Rizz
olatti (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” n
eurons 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 bodil
y state of pain as well as
anticipation of pain in a loved one activate
d

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 Emo
tional 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
th
e right in processing
other forms of self
and other awareness.


Co
nclusion


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 sy
stem
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 emotion
al 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, lea
rning,
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 2005
b, pp.31
-
32
),
proposing in essence that there
is a
one
-
dimensional

basic evaluation system

gu
i
ding brain development
, with the (apparent)

Disgust: Sensory Affect or Primary Emo
tional 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 seco
ndary (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
reaso
ns to discuss which emotions should be
considered basic
.
Firstl
y, 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 environment
al
components in the ontogeny of basic emotions
,
the

consideration of developmental mecha
nisms

may lead to new ideas on the promotion
of healthy emotional development

in human children.


Disgust: Sensory Affect or Primary Emo
tional 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 Emo
tional System?


26

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