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The Orbitofrontal Cortex and Reward

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The primate orbitofrontal cortex contains the secondary taste cortex, in which the reward value of taste is represented. It also contains the secondary and tertiary olfactory cortical areas, in which information about the identity and also about the reward value of odors is represented. The orbitofrontal cortex also receives information about the sight of objects and faces from the temporal lobe cortical visual areas, and neurons in it learn and reverse the visual stimulus to which they respond when the association of the visual stimulus with a primary reinforcing stimulus (such as a taste reward) is reversed. However, the orbitofrontal cortex is involved in representing negative reinforcers (punishers) too, such as aversive taste, and in rapid stimulus-reinforcement association learning for both positive and negative primary reinforcers. In complementary neuroimaging studies in humans it is being found that areas of the orbitofrontal cortex (and connected subgenual cingulate cortex) are activated by pleasant touch, by painful touch, by rewarding and aversive taste, and by odor. Damage to the orbitofrontal cortex in humans can impair the learning and reversal of stimulus- reinforcement associations, and thus the correction of behavioral responses when these are no longer appropriate because previous reinforcement contingencies change. This evidence thus shows that the orbitofrontal cortex is involved in decoding and representing some primary reinforcers such as taste and touch; in learning and reversing associations of visual and other stimuli to these primary reinforcers; and in controlling and correcting reward-related and punishment-related behavior, and thus in emotion.
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The primate orbitofrontal cortex contains the secondary taste cortex,
in which the reward value of taste is represented. It also contains the
secondary and tertiary olfactory cortical areas, in which information
about the identity and also about the reward value of odors is
represented. The orbitofrontal cortex also receives information about
the sight of objects and faces from the temporal lobe cortical visual
areas, and neurons in it learn and reverse the visual stimulus to
which they respond when the association of the visual stimulus with
a primary reinforcing stimulus (such as a taste reward) is reversed.
However, the orbitofrontal cortex is involved in representing negative
reinforcers (punishers) too, such as aversive taste, and in rapid
stimulus–reinforcement association learning for both positive and
negative primary reinforcers. In complementary neuroimaging
studies in humans it is being found that areas of the orbitofrontal
cortex (and connected subgenual cingulate cortex) are activated by
pleasant touch, by painful touch, by rewarding and aversive taste,
and by odor. Damage to the orbitofrontal cortex in humans can impair
the learning and reversal of stimulus– reinforcement associations,
and thus the correction of behavioral responses when these are no
longer appropriate because previous reinforcement contingencies
change. This evidence thus shows that the orbitofrontal cortex is
involved in decoding and representing some primary reinforcers such
as taste and touch; in learning and reversing associations of visual
and other stimuli to these primary reinforcers; and in controlling and
correcting reward-related and punishment-related behavior, and thus
in emotion.
The prefrontal cortex is the cortex that receives projections from
the mediodorsal nucleus of the thalamus and is situated in front
of the motor and premotor cortices (areas 4 and 6) in the frontal
lobe. Based on the divisions of the mediodorsal nucleus, the pre-
frontal cortex may be divided into three main regions (Fuster,
1997). First, the magnocellular, medial, part of the mediodorsal
nucleus projects to the orbital (ventral) surface of the prefrontal
cortex (which includes areas 13 and 12). This part of the
prefrontal cortex is called the orbitofrontal cortex, and receives
information from the ventral or object-processing visual stream,
and taste, olfactory and somatosensory inputs. Second, the
parvocellular, lateral, part of the mediodorsal nucleus projects
to the dorsolateral prefrontal cortex. This part of the prefrontal
cortex receives inputs from the parietal cortex and is involved in
tasks such as spatial short-term memory tasks (Fuster, 1997; Rolls
and Treves, 1998). Third, the pars paralamellaris (most lateral)
part of the mediodorsal nucleus projects to the frontal eye fields
(area 8) in the anterior bank of the arcuate sulcus.
The functions of the orbitofrontal cortex are considered in
this paper. The cortex on the orbital surface of the frontal lobe
includes area 13 caudally and area 14 medially, and the cortex
on the inferior convexity includes area 12 caudally and area 11
anteriorly (Fig. 1) (Carmichael and Price, 1994; Petrides and
Pandya, 1994; Price et al., 1996). This brain region is well dev-
eloped in primates, including humans, but poorly developed in
rodents, with homologies to areas found in primates uncertain,
so that care must be used in interpretation of the term ‘orbito-
frontal’ when applied to rodents (Uylings and van Eden, 1990).
To understand the function of this brain region in humans, the
majority of the studies described were therefore performed with
macaques or with humans.
Connections
Rolls et al. (1990) discovered an area with taste-responsive
neurons in the lateral part of the orbitofrontal cortex, and
showed that this was the secondary taste cortex in that it
receives a major projection from the primary taste cortex and
not from the thalamic taste relay nucleus (VPMpc) (Baylis et
al., 1994). More medially, there is an olfactory area (Rolls and
Baylis, 1994). Anatomically, there are direct connections from
the primary olfactory cortex (pyriform cortex) to area 13a of
the posterior orbitofrontal cortex, which in turn has onward
projections to a middle part of the orbitofrontal cortex (area 11)
(Morecraft et al., 1992; Barbas, 1993; Carmichael et al., 1994)
(Figs 1 and 2). Visual inputs reach the orbitofrontal cortex
directly from the inferior temporal cortex, in which repres-
entations of objects are found (Booth and Rolls, 1998), the
cortex in the anterior part of the superior temporal sulcus,
in which face-responsive neurons are found (Hasselmo et al.,
1989a,b; Wallis and Rolls, 1997), and the temporal pole (Barbas,
1988, 1993, 1995; Barbas and Pandya, 1989; Seltzer and Pandya,
1989; Morecraft et al., 1992; Carmichael and Price, 1995). There
are corresponding auditory inputs from the superior temporal
cortex (Barbas, 1988, 1993), and somatosensory inputs from
somatosensory cortical areas 1, 2 and SII in the frontal and
pericentral operculum, and from the insula (Barbas, 1988;
Carmichael and Price, 1995). The caudal orbitofrontal cortex
receives strong inputs from the amygdala (Price et al., 1991). The
orbitofrontal cortex also receives inputs via the mediodorsal
nucleus of the thalamus, the pars magnocellularis, which itself
receives afferents from temporal lobe structures such as the
prepyriform (olfactory) cortex, amygdala and inferior temporal
cortex (Price, 1999). The orbitofrontal cortex projects back to
temporal lobe areas such as the inferior temporal cortex and, in
addition, to the entorhinal cortex (or ‘gateway to the hippo-
campus’) and cingulate cortex (Insausti et al., 1987). The
orbitofrontal cortex also projects to the preoptic region and
lateral hypothalamus, the ventral tegmental area (Nauta, 1964;
Johnson et al., 1968), and the head of the caudate nucleus
(Kemp and Powell, 1970). Reviews of the cytoarchitecture and
connections of the orbitofrontal cortex are provided elsewhere
(Carmichael and Price, 1994, 1995; Petrides and Pandya, 1994;
Barbas, 1995; Pandya and Yeterian, 1996; Price, 1999).
The Orbitofrontal Cortex and Reward
Edmund T. Rolls
University of Oxford, Department of Experimental Psychology,
South Parks Road, Oxford OX1 3UD, UK
Cerebral Cortex Mar 2000;10:284–294; 1047–3211/00/$4.00
© Oxford University Press 2000
Effects of Lesions of the Orbitofrontal Cortex
Macaques with lesions of the orbitofrontal cortex are impaired at
tasks which involve learning about which stimuli are rewarding
and which are not, and especially in altering behavior when
reinforcement contingencies change. The monkeys may respond
when responses are inappropriate, e.g. no longer rewarded, or
may respond to a non-rewarded stimulus. For example, monkeys
with orbitofrontal damage are impaired on go/no-go task
performance, in that they go on the no-go trials (Iversen and
Mishkin, 1970); in an object reversal task, in that they respond to
the object which was formerly rewarded with food; and in
extinction, in that they continue to respond to an object which
is no longer rewarded (Butter, 1969; Jones and Mishkin, 1972).
There is some evidence for dissociation of function within the
orbitofrontal cortex, in that lesions to the inferior convexity
produce the go/no-go and object reversal deficits, whereas
damage to the caudal orbitofrontal cortex, area 13, produces the
extinction deficit (Rosenkilde, 1979).
Lesions produced more laterally, e.g. in the inferior convexity,
can influence working memory tasks in which objects must be
remembered for short periods, e.g. delayed matching to sample
and delayed matching to non-sample tasks (Passingham, 1975;
Mishkin and Manning, 1978; Kowalska et al., 1991), and neurons
in this region may help to implement this visual object
short-term memory by holding the representation active during
the delay period (Rosenkilde et al., 1981; Wilson et al., 1993) by
using the attractor properties of autoassociation networks (Rolls
and Treves, 1998; Renart et al., 1999). Whether this inferior
convexity area is specifically involved in a short-term object
memory is not yet clear, and a medial part of the frontal cortex
may also contribute to this function (Kowalska et al., 1991). It
should be noted that this short-term memory system for objects
(which receives inputs from the temporal lobe visual cortical
areas in which objects are represented) is different to the short-
term memory system in the dorsolateral part of the prefrontal
cortex, which is concerned with spatial short-term memories,
consistent with the inputs to the dorsolateral prefrontal cortex
from the parietal cortex, but also probably operates using the
attractor properties of autoassociation networks [in ways de-
scribed elsewhere (Rolls and Treves, 1998)].
Damage to the caudal orbitofrontal cortex in the monkey
also produces emotional changes (e.g. decreased aggression to
humans and to stimuli such as a snake and a doll), and a reduced
tendency to reject foods such as meat (Butter et al., 1969, 1970;
Butter and Snyder, 1972) or to display the normal preference
ranking for different foods (Baylis and Gaffan, 1991). In humans,
euphoria, irresponsibility and lack of affect can follow frontal
lobe damage (Damasio, 1994; Kolb and Whishaw, 1996; Rolls,
1999a), particularly orbitofrontal damage (Rolls et al.,1994;
Hornak et al., 1996).
Neurophysiology of the Orbitofrontal Cortex
Taste
One of the recent discoveries that has helped us to understand
the functions of the orbitofrontal cortex in behavior is that it
contains a major cortical representation of taste (Rolls, 1989,
1995a, 1997a) (cf. Fig. 2). Given that taste can act as a primary
reinforcer, i.e. as a reward or punishment innately without the
need for learning, we now have the start for a fundamental
understanding of the function of the orbitofrontal cortex in
stimulus–reinforcement association learning. We know how one
class of primary reinforcers reaches and is represented in the
orbitofrontal cortex. A representation of primary reinforcers is
essential for a system that is involved in learning associations
between previously neutral stimuli and primary reinforcers, e.g.
between the sight of an object and its taste. [In this paper, the
terms ‘reward and ‘positive reinforcer’ are used equivalently,
and are stimuli which an animal will work to obtain. Similarly,
the terms ‘punisher and ‘negative reinforcer’ are used to
describe stimuli that an animal will work to escape from or
avoid. A more detailed description is provided elsewhere (Rolls,
1999a, 2000b).]
The representation (shown by analyzing the responses of
single neurons in macaques) of taste in the orbitofrontal cortex
includes robust representations of the prototypical tastes sweet,
salty, bitter and sour (Rolls et al., 1990), but also separate
representations of the taste of water (Rolls et al., 1990), of
protein or umami as exemplified by monosodium glutamate
(Baylis and Rolls, 1991) and inosine monophosphate (Rolls et al.,
1996a, 1998), and of astringency as exemplified by tannic acid
(Critchley and Rolls, 1996c). All of these tastes are rewards or
punishers, i.e. reinforcers (Rolls, 1999a), and it is important to
realize that it is not just some general ‘reward’ that is represented
in the orbitofrontal cortex, but instead a very detailed and
information-rich representation of which particular reward or
punisher is present (as shown by the tuning curves for neurons
responding preferentially to each of the tastes described in the
Figure 1. Schematic diagram showing some of the gustatory, olfactory, visual and
somatosensory pathways to the orbitofrontal cortex, and some of the outputs of the
orbitofrontal cortex. The secondary taste cortex and the secondary olfactory cortex are
within the orbitofrontal cortex. V1, primary visual cortex. V4, visual cortical area V4.
Abbreviations: as, arcuate sulcus; cc, corpus callosum; cf, calcarine fissure; cgs,
cingulate sulcus; cs, central sulcus; ls, lunate sulcus; ios, inferior occipital sulcus; mos,
medial orbital sulcus; os, orbital sulcus; ots, occipito-temporal sulcus; ps, principal
sulcus; rhs, rhinal sulcus; sts, superior temporal sulcus; lf, lateral (or Sylvian) fissure
(which has been opened to reveal the insula); A, amygdala; INS, insula; T, thalamus; TE
(21), inferior temporal visual cortex; TA (22), superior temporal auditory association
cortex; TF and TH, parahippocampal cortex; TG, temporal pole cortex; 12, 13, 11,
orbitofrontal cortex; 35, perirhinal cortex; 51, olfactory (prepyriform and peri-
amygdaloid) cortex. Most of the forward projections shown in this diagram have
corresponding backprojections (Rolls and Treves, 1998).
Cerebral Cortex Mar 2000, V 10 N 3 285
papers just cited). This is essential given that a choice must
continually be made of which reinforcer to work for (or avoid),
depending on current need (e.g. homeostatic) states and also on
what rewards have been received recently (Rolls, 1999a, 2000c).
There is direct evidence that the reward value of taste is
represented in the orbitofrontal cortex. Part of the evidence is
that the responses of orbitofrontal taste neurons are modulated
by hunger (as is the reward value or palatability of a taste).
In particular, it has been shown that orbitofrontal cortex taste
neurons stop responding to the taste of a food with which the
monkey is fed to satiety (Rolls et al., 1989). In contrast, the re-
presentation of taste in the primary taste cortex (Scott et al.,
1986; Yaxley et al., 1990) is not modulated by hunger (Rolls et
al., 1988; Yaxley et al., 1988). This finding shows that in the
primary taste cortex the reward value of taste is not represented,
but instead the identity of the taste is represented. Additional
evidence that the reward value of food is represented in the
orbitofrontal cortex is that monkeys work for electrical stimu-
lation of this brain region if they are hungry, but not if they are
satiated (Mora et al., 1979; Rolls, 1999a). Further, neurons in the
orbitofrontal cortex are activated from many brain-stimulation
reward sites (Mora et al., 1980; Rolls et al., 1980). Thus there is
clear evidence that it is the reward value of taste that is repres-
ented in the orbitofrontal cortex (Rolls, 1999a).
The secondary taste cortex is in the caudolateral part of the
orbitofrontal cortex, as defined anatomically (Baylis et al., 1994).
This region projects onto other regions in the orbitofrontal
cortex (Baylis et al., 1994), and neurons with taste responses
(in what can be considered as a tertiary gustatory cortical area)
can be found in many regions of the orbitofrontal cortex (Rolls
et al., 1990, 1996b; Rolls and Baylis, 1994). Neurons from these
regions project to the hypothalamus and the basal forebrain, and
it is probably by this route that hypothalamic neurons receive the
inputs which make them respond to the taste and/or sight of
food if the monkey is hungry (Fig. 2) (Rolls et al., 1986; Rolls,
1999a).
Convergence of Taste and Olfactory Inputs in the
Orbitofrontal Cortex: the Representation of Flavor
In these regions of the orbitofrontal cortex, not only unimodal
taste neurons but also unimodal olfactory neurons are found.
In addition, some single neurons respond to both gustatory and
olfactory stimuli, often with correspondence of tuning between
the two modalities (Rolls and Baylis, 1994) (cf. Fig. 2). For
example, some neurons respond to the taste of glucose and to
the odor of banana. Other neurons respond to salty taste or to
savory odours. It is probably here in the orbitofrontal cortex of
primates that these two modalities converge to produce the
representation of flavor (Rolls and Baylis, 1994). Evidence will
soon be described that indicates that these representations are
built by olfactory–gustatory association learning, an example
Figure 2. Schematic diagram showing some of the gustatory, olfactory, visual and somatosensory pathways to the orbitofrontal cortex, and some of the outputs of the orbitofrontal
cortex. The secondary taste cortex and the secondary olfactory cortex are within the orbitofrontal cortex. V1, primary visual cortex. V4, visual cortical area V4. The gate function refers
to the fact that neurons in the orbitofrontal cortex and lateral hypothalamus only respond to the sight, taste or smell of food if hunger signals are present (Rolls, 1997a, 1999a).
286 The Orbitofrontal Cortex Rolls
of stimulus–reinforcement (e.g. stimulus–reward) association
learning.
An Olfactory Representation in the Orbitofrontal Cortex
Takagi, Tanabe and colleagues (Takagi, 1991) described single
neurons in the macaque orbitofrontal cortex that were activated
by odors. A ventral frontal region has been implicated in olfact-
ory processing in humans (Jones-Gotman and Zatorre, 1988;
Zatorre and Jones-Gotman, 1991; Zatorre et al., 1992). Rolls and
colleagues have analyzed the rules by which orbitofrontal
olfactory representations are formed and operate in primates.
For 35% of neurons in the orbitofrontal olfactory areas, Critchley
and Rolls (Critchley and Rolls, 1996a) showed that the repres-
entation of the olfactory stimulus depended on its association
with taste reward (analyzed in an olfactory discrimination task
with taste reward). For the remaining 65% of the neurons, the
odors to which a neuron responded were not influenced by the
taste (glucose or saline) with which the odor was associated.
Thus the odor representation for 35% of orbitofrontal neurons
appeared to be built by olfactory to taste association learning,
where the taste is a primary rewarding or punishing stimulus.
This possibility was confirmed by reversing the taste with which
an odor was associated in the reversal of an olfactory discrim-
ination task. It was found that 68% of the sample of neurons
analyzed altered the way in which they responded to odor when
the taste reinforcement association of the odor was reversed
(Rolls et al., 1996b). (Of the 68%, 25% showed reversal and
43% no longer discriminated after the reversal. The olfactory to
taste reversal was quite slow, both neurophysiologically and
behaviorally, often requiring 20–80 trials, consistent with the
need for some stability of flavor representations. The relatively
high proportion of neurons with modification of responsive-
ness by taste association was probably related to the fact that
the neurons were preselected to show differential responses to
the odors associated with different tastes in the olfactory dis-
crimination task.) Thus the rule according to which the orbito-
frontal olfactory representation is formed is for some neurons by
association learning with taste reward or punishment.
To analyze the nature of the olfactory representation in the
orbitofrontal cortex, Critchley and Rolls measured the responses
of olfactory neurons that responded to food while they fed the
monkey to satiety (Critchley and Rolls, 1996b). They found that
the majority of orbitofrontal olfactory neurons decreased their
responses to the odor of the food (e.g. fruit juice) with which the
monkey was fed to satiety. Thus for these neurons the reward
value of the odor is what is represented in the orbitofrontal
cortex. These sensory-specific decreases in neuronal responses
to odors produced by feeding to satiety with a particular food
follow closely the sensory-specific decrease in the pleasantness
of the odor of a food produced by feeding to satiety in humans
(Rolls and Rolls, 1997). We do not yet know whether this is the
first stage of processing at which reward value is represented
in the olfactory system [although in rodents the inf luence of
reward association learning appears to be present in some
neurons in the pyriform cortex (Schoenbaum and Eichenbaum,
1995)].
An important principle in the representation of reward in the
orbitofrontal cortex is that not only is there a detailed repres-
entation of different rewarding stimuli (including olfactory,
taste, visual and texture stimuli), but also the reward value of
each stimulus is updated continually. This is shown by experi-
ments on sensory-specific satiety, in which individual neurons
stop responding to the food on which a monkey is satiated in
parallel with the decrease in its reward value, but continue to
respond to the other stimuli to which they are tuned which
remain rewarding (Rolls et al., 1989, 1999a; Critchley and Rolls,
1996b; Rolls, 1999a). Sensory-specific satiety is computed by
these neurons in the primate orbitofrontal cortex (Rolls and
Treves, 1998; Rolls, 1999a), in that effects of satiety on neuronal
responses to sensory stimuli are not found in the primary
taste cortex (Rolls et al., 1988; Yaxley et al., 1988) or in the
inferior temporal visual cortex (Rolls et al., 1977). This rich
representation provided by ensembles of orbitofrontal cortex
neurons, each tuned to different sets of olfactory, taste, visual
and tactile stimuli and providing detailed information about
stimuli for which an animal might work, is very different from
that provided by dopamine neurons (Schultz et al., 1995), the
activity of which ref lects what the animal does rather than the
information about the reward value of a wide range of stimuli
on the basis of which a decision might be taken (Rolls, 1999a,
2000b). Indeed, in that dopamine release occurs to aversive as
well as to rewarding stimuli to which an animal performs actions
(Gray et al., 1997), it has been suggested that the dopamine
system may be related to processing which ref lects whether a
behavioral response should be, or is being, performed rather
than to reward per se (Rolls, 1999a, 2000b). A way to investigate
this further would be to record from dopamine neurons, as well
as to measure dopamine release from the terminal areas, when
monkeys initiate active responses in order to avoid aversive
stimuli (Rolls, 2000b).
Although individual neurons do not encode large amounts of
information about which of 7–9 odors has been presented, we
have shown that the information does increase linearly with the
number of neurons in the sample (Rolls et al., 1996c). This
ensemble encoding results in useful amounts of information
about which odor has been presented being provided by orbito-
frontal olfactory neurons.
Visual Inputs to the Orbitofrontal Cortex, and Visual
Stimulus–Reinforcement Association Learning and
Reversal
We have been able to show that there is a major visual input to
many neurons in the orbitofrontal cortex, and that what is
represented by these neurons is in many cases the reinforcement
association of visual stimuli. The visual input is from the ventral,
temporal lobe, a visual stream concerned with ‘what’ object is
being seen in that orbitofrontal visual neurons frequently re-
spond differentially to objects or images depending on their
reward association (Thorpe et al., 1983; Rolls et al., 1996b). The
primary reinforcer that has been used is taste. Many of these
neurons show visual–taste reversal in one or a very few trials
(e.g. Fig. 3). (In a visual discrimination task they will reverse the
stimulus to which they respond, e.g. from a triangle to a square,
in one trial when the taste delivered for a behavioral response to
that stimulus is reversed.) This reversal learning probably occurs
in the orbitofrontal cortex, for it does not occur one synapse
earlier in the visual inferior temporal cortex (Rolls et al., 1977),
and it is in the orbitofrontal cortex that there is convergence of
visual and taste pathways onto the same neurons (Thorpe et al.,
1983; Rolls and Baylis, 1994; Rolls et al., 1996a). The probable
mechanism for this learning is Hebbian modification of synapses
conveying visual input onto taste-responsive neurons, imple-
menting a pattern association network (Rolls and Treves, 1998;
Rolls, 1999a). Further evidence that the visual responses of these
neurons ref lect the reward value of the visual stimuli is that
these neurons respond to the sight of a particular food when the
Cerebral Cortex Mar 2000, V 10 N 3 287
monkey is hungry but not when satiated (Critchley and Rolls,
1996b). In doing this, the neurons show sensory-specific satiety,
continuing to respond to the sight of other foods which are still
rewarding because they have not been fed to satiety (Critchley
and Rolls, 1996b). The fact that the responses of these visual
neurons in the orbitofrontal cortex reflect the reward value and
not the physical properties of the visual stimuli (Thorpe and
Rolls, 1983; Rolls et al., 1996b; Critchley and Rolls, 1996b) has
been confirmed by Tremblay and Schultz (1999).
In addition to these neurons that encode the reward
association of visual stimuli, other neurons in the orbitofrontal
cortex detect non-reward, in that they respond for example
when an expected reward is not obtained when a visual discrim-
ination task is reversed (Thorpe et al., 1983). Different
populations of such neurons respond to other types of non-
reward, including the removal of a formerly approaching taste
reward and the termination of a taste reward (Thorpe et al.,
1983). The presence of these neurons is fully consistent with the
hypothesis that they are part of the mechanism by which the
orbitofrontal cortex enables very rapid reversal of behavior by
stimulus–reinforcement association relearning when the associa-
tion of stimuli with reinforcers is altered or reversed (Rolls,
1986a, 1990). Different orbitofrontal cortex neurons respond to
different types of non-reward (Thorpe et al., 1983), potentially
enabling task- or context-specific reversal to occur.
Another type of information represented in the orbitofrontal
cortex is information about faces. There is a population of orbito-
frontal neurons which respond in many ways similar to those in
the temporal cortical visual areas, the properties of which are
described elsewhere (Rolls, 1984, 1992a, 1994a, 1995b, 1996a,
1997b; Wallis and Rolls, 1997). The orbitofrontal face responsive
neurons, first observed by Thorpe et al. (Thorpe et al., 1983)
then by Rolls et al. (Booth et al., 1998; Rolls, 1999a; Rolls et al.,
2000), tend to respond with longer latencies than temporal lobe
neurons (130–220 ms typically, compared with 80–100 ms);
they also convey information about which face is being seen, by
having different responses to different faces, and are typically
rather harder to activate strongly than temporal cortical face-
selective neurons, in that many of them respond much better to
real faces than to two-dimensional images of faces on a video
monitor (Rolls and Baylis, 1986). Some of the orbitofrontal
cortex face-selective neurons are responsive to face gesture or
movement. The findings are consistent with the likelihood that
these neurons are activated via the inputs from the temporal
cortical visual areas in which face-selective neurons are found
(see Fig. 2). The significance of the neurons is likely to be related
to the fact that faces convey information that is important in
social reinforcement. One way in which these neurons carry
useful information in such situations is that by encoding face
expression (Hasselmo et al., 1989) (e.g. a smile or angry ex-
pression), their activation can act as a reinforcer. This may be
partly innate and partly by association with a primary reinforcer
such as a pleasant touch or pain. Another way in which face-
selective neurons may carry useful information in such situ-
ations is that they encode information about which individual is
present (Hasselmo et al., 1989), which is also important in social
situations as learned associations of particular individuals with
reinforcers such as touch or pain can again guide behavior.
Indeed, in primate social interactions, individuals are constantly
updating their evaluation of other individuals in terms of the
reinforcers received, and rapid learning of associations between
representations of face identity and reinforcers in the primate
orbitofrontal cortex is likely to be part of this process.
Somatosensory Inputs to the Orbitofrontal Cortex
Some neurons in the macaque orbitofrontal cortex respond to
the texture of food in the mouth. Some neurons alter their
responses when the texture of a food is modified by adding
gelatine or methyl cellulose, or by partially liquefying a solid
food such as apple (Critchley et al., 1993). Another population
of orbitofrontal neurons responds when a fatty food such as
cream is in the mouth. These neurons can also be activated by
pure fat, such as glyceryl trioleate, and by non-fat substances
with a fat-like texture, such as paraffin oil (hydrocarbon) and
silicone oil (Si(CH
3
)
2
O)
n
). These neurons thus provide informa-
tion by somatosensory pathways that a fatty food is in the mouth
(Rolls et al., 1999a). These inputs are perceived as pleasant when
hungry, because of the utility of ingestion of foods which are
likely to contain essential fatty acids and to have a high calorific
value (Rolls, 1999a,c). In addition to these oral somatosensory
inputs to the orbitofrontal cortex, there are also somatosensory
inputs from other parts of the body, and indeed an investigation
we have performed with functional magnetic resonance imaging
(fMRI) in humans indicates that pleasant and painful touch
stimuli to the hand produce greater activation of the orbito-
frontal cortex relative to the somatosensory cortex than do
affectively neutral stimuli (Rolls et al., 1997a; Francis et al.,
1999) (see below).
Figure 3. Visual discrimination reversal of the responses of a single neuron in the
macaque orbitofrontal cortex when the taste with which the two visual stimuli (a
triangle and a square) were associated was reversed. Each point is the mean
poststimulus firing rate measured in a 0.5 s period over 10 trials to each of the stimuli.
Before reversal, the neuron fired most to the square when it indicated (S+) that the
monkey could lick to obtain a taste of glucose. After reversal, the neuron responded
most to the triangle when it indicated that the monkey could lick to obtain glucose. The
response was low to the stimuli when they indicated (S–) that if the monkey licked then
aversive saline would be obtained. (b) The behavioral response to the triangle and the
square, indicating that the monkey reversed rapidly (Rolls et al., 1996).
288 The Orbitofrontal Cortex Rolls
A Neurophysiological Basis for Stimulus–Reinforcement Learning
and Reversal in the Orbitofrontal Cortex
The neurophysiological evidence and the effects of lesions
described suggests that one function implemented by the
orbitofrontal cortex is rapid stimulus–reinforcement associ-
ation learning, and the correction of these associations when
reinforcement contingencies in the environment change. To
implement this, the orbitofrontal cortex has the necessary
representation of primary reinforcers, including taste and
somatosensory stimuli. It also receives information about ob-
jects, e.g. visual view-invariant information (Booth and Rolls,
1998), and can associate this at the neuronal level with primary
reinforcers such as taste and reverse these associations very
rapidly. Another type of stimulus which can be conditioned in
this way in the orbitofrontal cortex is olfactory, although here
the learning is slower. It is likely that auditory stimuli can be
associated with primary reinforcers in the orbitofrontal cortex,
though there is less direct evidence of this yet. The orbitofrontal
cortex also has neurons which detect non-reward, which are
likely to be used in behavioral extinction and reversal. They may
do this not only by helping to reset the reinforcement association
of neurons in the orbitofrontal cortex, but also by sending a
signal to the striatum which could be routed by the striatum
to produce appropriate behaviors for non-reward (Rolls and
Johnstone, 1992; Williams et al., 1993; Rolls, 1994b). Indeed, the
striatal route may be an important one through which the
orbitofrontal cortex influences behavior when the orbitofrontal
cortex is decoding reinforcement contingencies and their
changes (Rolls, 1999a). Some of the evidence for this is that
neurons with responses that ref lect the output of orbitofrontal
neurons are found in the ventral part of the head of the caudate
nucleus (Rolls et al., 1983a) and the ventral striatum (Rolls and
Williams, 1987; Schultz et al., 1992; Williams et al., 1993) —
parts of the striatum that receive connections from the orbito-
frontal cortex — and that lesions of the ventral part of the head of
the caudate nucleus impair visual discrimination reversal (Divac
et al., 1967), which is also impaired by orbitofrontal cortex
lesions. The relation between orbitofrontal cortex and striatal
processing is considered further elsewhere (Rolls and Johnstone,
1992; Rolls, 1994b, 1999a; Rolls and Treves, 1998).
Decoding the reinforcement value of stimuli, which involves
for previously neutral (e.g. visual) stimuli learning their
association with a primary reinforcer, often rapidly, and which
may involve not only rapid learning but also rapid relearning
and alteration of responses when reinforcement contingencies
change, is then a function proposed for the orbitofrontal cortex.
Using this decoding to specify the goals for action would be
important in, for example, motivational and emotional behavior.
It would be important in, for example, feeding and drinking by
enabling primates to learn rapidly about the food reinforcement
to be expected from visual stimuli (Rolls, 1994c, 1999a). This
is important, for primates frequently eat more than 100 vari-
eties of food; vision by visual–taste association learning can
be used to identify when foods are ripe; and during the course
of a meal, the pleasantness of the sight of a food eaten in the
meal decreases in a sensory-specific way (Rolls et al., 1983b),
a function that is probably implemented by the sensory-
specific satiety-related responses of orbitofrontal visual neurons
(Critchley and Rolls, 1996b).
With respect to emotional behavior, decoding and rapidly
readjusting the reinforcement value of visual signals is likely to
be crucial, for emotions can be described as states elicited by
reinforcing signals (Rolls, 1986a,b, 1990, 1995b, 1999a, 2000b).
For example, fear is a state produced by a stimulus or event
associated with a punisher such as pain. The ability to perform
this learning very rapidly is probably very important in social
situations in primates, in which reinforcing stimuli are continu-
ally being exchanged, and the reinforcement value of stimuli
must be continually updated (relearned), based on the actual
reinforcers received and given. Although the functions of the
orbitofrontal cortex in implementing the operation of re-
inforcers such as taste, smell, tactile and visual stimuli including
faces are most understood, in humans the rewards processed in
the orbitofrontal cortex include quite general learned rewards
(i.e. secondary reinforcers) such as working for ‘points’, as will
be described shortly.
Although the amygdala is concerned with some of the same
functions as the orbitofrontal cortex, and receives similar inputs
(see Fig. 2), there is evidence that it may function less effectively
in the very rapid learning and reversal of stimulus reinforcement
associations, as indicated by the greater difficulty in obtaining
reversal from amygdala neurons (Sanghera et al., 1979; Rolls,
1992b, 2000a; Wilson and Rolls, 2000), and by the greater effect
of orbitofrontal lesions in leading to continuing choice of no
longer rewarded stimuli (Jones and Mishkin, 1972). In primates,
the necessity for very rapid stimulus–reinforcement re-evalua-
tion and the development of powerful cortical learning systems
may result in the orbitofrontal cortex effectively taking over this
aspect of amygdala functions (Rolls, 1992b, 1999a, 2000a).
The Human Orbitofrontal Cortex
It is of interest that a number of the symptoms of damage to some
parts of the frontal lobes in humans appear to be related to the
type of function just described, namely altering behavior when
stimulus–reinforcement associations alter, as described next.
Thus, some humans with frontal lobe damage can show impair-
ments in a number of tasks in which an alteration of behavioral
strategy is required in response to a change in environmental
reinforcement contingencies (Goodglass and Kaplan, 1979;
Jouandet and Gazzaniga, 1979; Eslinger and Grattan, 1993; Kolb
and Whishaw, 1996). For example, Milner showed that in the
Wisconsin Card Sorting Task (in which cards are to be sorted
according to the color, shape or number of items on each card
depending on whether the examiner says ‘right’ or ‘wrong’ to
each placement), some frontal patients had difficulty either in
determining the first sorting principle or in shifting to a second
principle when required to (Milner, 1963). Also, in stylus mazes,
frontal patients have difficulty in changing direction when a
sound indicates that the correct path has been left (Milner,
1982). It is of interest that, in both types of test, frontal patients
may be able to verbalize the correct rules yet be unable to
correct their behavioral sets or strategies appropriately. Some of
the personality changes that can follow frontal lobe damage may
also be related to a dysfunction in the alteration of stimulus–
reinforcer associations. For example, the euphoria, irresponsi-
bility, lack of affect and lack of concern for the present or future
which can follow frontal lobe damage (Hecaen and Albert, 1978;
Damasio, 1994) may also be related to a dysfunction in altering
behavior appropriately in response to a change in reinforcement
contingencies. Indeed, insofar as the orbitofrontal cortex is
involved in the disconnection of stimulus–reinforcer associ-
ations, and such associations are important in learned emotional
responses (above), then it follows that the orbitofrontal cortex
is involved in emotional responses by correcting stimulus
reinforcer associations when they become inappropriate.
These hypotheses, and the role in particular of the orbito-
Cerebral Cortex Mar 2000, V 10 N 3 289
frontal cortex in human behavior, have been investigated in
recent studies in humans with damage to the ventral parts of the
frontal lobe. (The description ‘ventral’ is given to indicate that
there was pathology in the orbitofrontal or related parts of the
frontal lobe but not in the more dorsolateral parts of it.) A task
which was designed to directly assess the rapid alteration of
stimulus–reinforcement associations was used, because the
findings above indicate that the orbitofrontal cortex is involved
in this type of learning. This task was used instead of the
Wisconsin Card Sorting Task, which requires patients to shift
from category (or dimension) to category, e.g. from color to
shape, and clearly requires cognitive processing that is different
from or additional to the stimulus–reinforcement association
learning in which the orbitofrontal cortex is implicated. The
task used was visual discrimination reversal, in which patients
could learn to obtain points by touching one stimulus when it
appeared on a video monitor but had to withhold a response
when a different visual stimulus appeared, otherwise a point was
lost. After the subjects had acquired the visual discrimina- tion,
the reinforcement contingencies unexpectedly reversed. The
patients with ventral frontal lesions made more errors in
the reversal task (or in a similar extinction task in which the
reward was no longer given), and completed fewer reversals,
than control patients with damage elsewhere in the frontal lobes
or in other brain regions (Rolls et al., 1994). The impairment
correlated statistically significantly with the socially inappropri-
ate or disinhibited behavior of the patients (assessed in a
Behavior Questionnaire) (Spearman ρ = 0.76, P = 0.002) (Rolls
et al., 1994). The patients were not impaired at other types of
memory task, such as paired associate learning. The continued
choice of the no-longer-rewarded stimulus in the reversal of the
visual discrimination task is interpreted as a failure to reverse
stimulus–reinforcer, that is, sensory–sensory, associations, and
not as the motor response perseveration which may follow much
more dorsal damage to the frontal lobes, and this is being
investigated further in this type of patient. However, I note that
one of the types of evidence which bears very directly on this
comes from the responses of orbitofrontal cortex neurons in
macaques. The evidence comes from the orbitofrontal cortex
neurons that respond in relation to a sensory stimulus such as a
visual stimulus when it is paired with another sensory stimulus
to which the neuron responds such as a taste stimulus (Thorpe
et al., 1983; Rolls et al., 1996b). The taste stimulus is a primary
reinforcer. These neurons do not respond in relation to motor
responses, and could not be involved in stimulus-to-motor
response association learning. Bechara and colleagues also have
findings that are consistent with these in patients with frontal
lobe damage when they perform a gambling task (Bechara et al.,
1994, 1996, 1997; Damasio, 1994). The patients could choose
cards from different decks. The patients with frontal damage
were more likely to choose cards from a deck which gave
rewards with a reasonable probability but also had occasional
very heavy penalties, resulting in lower net gains than choices
from the other deck. In this sense, the patients were not affected
by the negative consequences of their actions: they did not
switch from the deck of cards which was providing significant
rewards even when large punishments were incurred.
It is of interest that in the reversal and extinction tasks the
patients can often verbalize the correct response yet commit the
incorrect action (Rolls et al., 1994). This is consistent with the
hypothesis that the orbitofrontal cortex is normally involved in
executing behavior when the behavior is performed by
evaluating the reinforcement associations of environmental
stimuli (below). The orbitofrontal cortex appears to be involved
in this in both humans and non-human primates, when the learn-
ing must be performed rapidly, e.g. in acquisition and during
reversal.
An idea of how such stimulus–reinforcer learning may play an
important role in normal human behavior, and may be related to
the behavioral changes seen clinically in these patients with
ventral frontal lobe damage, can be provided by summarizing the
behavioral ratings given by the carers of these patients. The
patients were rated high in the Behavior Questionnaire on at
least some of the following: disinhibited or socially inappropri-
ate behavior; misinterpretation of other people’s moods;
impulsiveness; unconcern or underestimation of the seriousness
of their condition; and lack of initiative (Rolls et al., 1994). Such
behavioral changes correlated statistically with the stimulus–
reinforcer reversal and extinction learning impairment (see
above) (Rolls et al., 1994). The suggestion thus is that the
insensitivity to reinforcement changes in the learning task may
be at least part of what produces the changes in behavior found
in these patients with ventral frontal lobe damage. The more
general impact on the behavior of these patients is that their
irresponsibility tended to affect their everyday lives. For ex-
ample, if such patients had received their brain damage in a road
traffic accident and compensation had been awarded, they often
tended to spend their money without appropriate concern for
the future, sometimes, for example, buying a very expensive car.
Such patients often find it difficult to invest in relationships too,
and are sometimes described by their family as having changed
personalities, in that they care less about a wide range of factors
than before the brain damage. The suggestion that follows from
this is that the orbitofrontal cortex may normally be involved in
much social behavior, and the ability to respond rapidly and
appropriately to social reinforcers is of course an important
aspect of primate (including human) social behavior.
To investigate the possible significance of face-related inputs
to orbitofrontal visual neurons described above, we also tested
the responses of these patients to faces. We included tests of face
(and also voice) expression decoding, because these are ways in
which the reinforcing quality of individuals is often indicated.
Impairments in the identification of facial and vocal emotional
expression were demonstrated in a group of patients with
ventral frontal lobe damage who had socially inappropriate
behavior (Hornak et al., 1996; Rolls, 1999b). The expression
identification impairments could occur independently of per-
ceptual impairments in facial recognition, voice discrimination
or environmental sound recognition. The face and voice ex-
pression problems did not necessarily occur together in the same
patients, providing an indication of separate processing. The
impairment was found on most expressions apart from happy
(which as the only positive face expression was relatively easily
discriminable from the others), with sad, angry, frightened and
disgusted showing lower identification than surprised and
neutral (Rolls, 1999b). Poor performance on both expression
tests was correlated with the degree of alteration of emotional
experience reported by the patients (Spearman ρ = 0.88, P <<
0.05). There was also a statistically strong positive correlation
between the degree of altered emotional experience and the
severity of the behavioral problems (e.g. disinhibition) found in
these patients (Hornak et al., 1996; Rolls, 1999b) (Spearman ρ =
0.66, P < 0.01). A comparison group of patients with brain
damage outside the ventral frontal lobe region, without these
behavioral problems, was unimpaired on the face expression
identification test, was significantly less impaired at vocal
290 The Orbitofrontal Cortex Rolls
expression identification and reported little subjective emotional
change (Hornak et al., 1996). These investigations are being
extended in current studies, and it is being found that patients
with face expression decoding problems do not necessarily have
impairments at visual discrimination reversal, and vice versa.
This is consistent with some topography in the orbitofrontal
cortex (Rolls and Baylis, 1994).
To elucidate the role of the human orbitofrontal cortex in
emotion further, Rolls, Francis et al. (Rolls et al., 1997a; Francis
et al., 1999) performed an investigation to determine where the
pleasant affective component of touch is represented in the
brain. Touch is a primary reinforcer that can produce pleasure.
They found with fMRI that a weak but very pleasant touch of the
hand with velvet produced much stronger activation of the
orbitofrontal cortex than a more intense but affectively neutral
touch of the hand with wood. In contrast, the affectively
neutral but more intense touch produced more activation of the
primary somatosensory cortex than the pleasant stimuli (Fig. 4).
These findings indicate that part of the orbitofrontal cortex is
concerned with representing the positively affective aspects
of somatosensory stimuli. The significance of this finding is
that a primary reinforcer that can produce affectively positive
emotional responses is represented in the human orbitofrontal
cortex. This provides one of the bases for the human orbito-
frontal cortex to be involved in the stimulus–reinforcement
association learning that provides the basis for emotional
learning. In more recent studies, we (Rolls, McGlone, Francis,
Bowtell and O’Doherty) are finding that there is also a repres-
entation of the affectively negative aspects of touch, including
pain, in the human orbitofrontal cortex. This is consistent with
findings that humans with damage to the ventral part of the
frontal lobe may report that they know that a stimulus is
pain-producing, but that the pain does not feel very bad to them
(Freeman and Watts, 1950; Valenstein, 1974; Melzack and Wall,
1996). It will be of interest to determine whether the regions of
the human orbitofrontal cortex that represent pleasant touch and
pain are close topologically or overlap. Even if fMRI studies show
that the areas overlap, it would nevertheless be the case that
different populations of neurons would be being activated, for
this is what recordings from single cells in monkeys indicate
about positively versus negatively affective taste, olfactory and
visual stimuli (above).
It is also of interest that nearby, but not overlapping, parts of
the human orbitofrontal cortex are activated by taste stimuli
(such as glucose) and by olfactory stimuli (such as vanilla) (Rolls
et al., 1997b; Francis et al., 1999). It is not yet known from
human fMRI studies whether it is the reinforcing aspects of taste
and olfactory stimuli that are represented here, but this is likely
in view of the findings in non-human primates (Rolls, 1999a)
and a recent paper showing orbitofrontal cortex activation in
humans that is related to olfactory sensory-specific satiety
(O’Doherty et al., 2000).
Conclusions
The investigations described here show that the primate orbito-
frontal cortex is involved in representing primary (unlearned)
reinforcers such as taste and touch, and in learning associations
of other stimuli, such as visual and olfactory stimuli, with these
primary reinforcers. For these reasons, the orbitofrontal cortex
has important functions in motivational behavior such as feeding
and drinking, and in emotion and social behavior (Rolls, 1999a).
The type of learning in which the orbitofrontal cortex is involved
is stimulus–reinforcer association learning, which is a particular
case of stimulus–stimulus association learning. The model for the
implementation is a pattern association between the conditioned
(to-be-learned, e.g. visual) stimulus, which activates the output
neurons through associatively modifiable synapses, and the
primary reinforcer, which activates the neurons through non-
modifiable synapses (Rolls and Treves, 1998). Once learned, the
same conditioned stimulus will activate the output neurons, with
no need for ongoing activity of neurons in order to implement
the memory. If the contingency reverses, the synapses from the
neurons representing the previous conditioned stimulus are no
longer active when the output neuron is active, and the synapses
become weaker by a process of heterosynaptic long-term depres-
sion (Rolls and Treves, 1998).
Stimulus–reinforcer association memory is distinct from the
type of working memory implemented in the dorsolateral and
inferior convexity prefrontal areas. The model for the imple-
mentation of such working memories is an autoassociation
neural network in which the memory state is kept active by
continuously recirculating neuronal activity implemented by
recurrent collateral associatively modifiable synapses between
the pyramidal cells (Rolls and Treves, 1998). The dorsolateral
part of the prefrontal cortex receives inputs particularly from
area 7 of the parietal cortex, and may be especially involved in
spatial response working memory; while the inferior convexity
prefrontal cortex receives activity particularly from the inferior
temporal visual cortex, and may be more involved in object
working memory (Fuster, 1997; Goldman-Rakic, 1996; Rolls and
Treves, 1998). The orbitofrontal cortex stimulus–reinforcer
pattern association memory is also very distinct from the
episodic declarative memory in which the hippocampal system
is implicated. This system may store memories by forming arbi-
trary associations between conjunctive events which need not
be reinforcers and which typically include a spatial component.
The storage may occur using an autoassociation network which
does not operate in a continuous attractor mode in order to store
a memory (Rolls, 1996b; Rolls and Treves, 1998).
One set of output pathways by which the orbitofrontal cortex
implements these functions for behavior is via the striatum
(Rolls, 1996a, 1999a). Another output of the orbitofrontal cortex
Figure 4. Histograms showing the mean (± SEM, across seven experiments) of the
change in activation of different brain regions during the pleasant and neutral
somatosensory stimulation. The histograms show the average activation bilaterally in
the orbitofrontal cortex and contralaterally to the stimulation for the somatosensory
cortex. The measure of activation for each region is the average percentage change in
activation in voxels with significant activation at the P < 0.005 level, multiplied by the
number of significant voxels. There was a significant interaction (P < 0.001) between
whether the touch was pleasant versus neutral and activation of the orbitofrontal cortex
versus somatosensory cortex (Francis et al., 1999).
Cerebral Cortex Mar 2000, V 10 N 3 291
is to the hypothalamus, and it is probably by this route that hypo-
thalamic neurons in primates come to respond to the sight and
taste of food when hunger is present [Fig. 2; further evidence is
presented elsewhere (Rolls, 1999a)]. The functions of this out-
put system, and the orbitofrontal cortex connections which are
directed further caudally in the brainstem, include autonomic
and endocrine responses learned and updated to changing
environmental stimuli (Rolls, 1999a).
Notes
The author has worked on some of the experiments described here
with L.L. Baylis, G.C. Baylis, R. Bowtell, A.D. Browning, H.D. Critchley,
S. Francis, M.E. Hasselmo, J. Hornak, C.M. Leonard, F. McGlone, F. Mora,
D.I. Perrett, T.R. Scott, S.J. Thorpe, E.A. Wakeman and F.A.W. Wilson,
and their collaboration is sincerely acknowledged. Some of the research
described was supported by the Medical Research Council, PG8513790.
Address correspondence to Edmund T. Rolls, University of Oxford,
Department of Experimental Psychology, South Parks Road, Oxford OX1
3UD, UK. Email: edmund.rolls@psy.ox.ac.uk.
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294 The Orbitofrontal Cortex Rolls
... Orbitofrontal cortex (OFC), the major recipient in the frontal lobe of both gustatory and olfactory information, is involved in flavor perception and executive functions of the two sensory modalities. In flavor perception, it integrates information of multiple sensory modalities such as gustatory, olfactory, and visual sensations [1][2][3] and also makes rapid stimulus-reinforcement association of multiple inputs [4,5]. In execution function, OFC has the ability to integrate and organize information in selection of behavioral strategies [6][7][8], and contributes to value evaluation and outcome prediction [9][10][11]. ...
Article
Full-text available
Orbitofrontal cortex (OFC) is involved in flavor perception and executive functions of chemical sensations. It integrates multiple sensory modalities to perceive the flavor of foods, and organizes sensory information in selection of behavioral strategies. A recent study has reported that gustatory working memory (WM) is maintained in the OFC of rhesus monkeys. However, the maintenance mechanism remains unclear. Moreover, the manipulation mechanism, or how WM is utilized to guide behavior, also poorly understood. To address these issues, we are concerned with a delayed match-to-sample (DMS) task, and present a model for WM maintenance and manipulation in OFC. The model consists of the networks of gustatory cortex, OFC, and a decision layer. We show that gustatory WM is represented by a sparse activity of OFC neurons, elicited by short-term synaptic plasticity. The intermittent spiking in the sparse activity prevents from reducing the efficacy of short-term synaptic plasticity. The sparse activity codes WM in a functionally latent state, and retrieves WM in a functionally active state as it is needed. In contrast, top-down signals from OFC allows GC neurons to represent the gustatory information relevant to the WM maintained in OFC. We also present a comparison mechanism of a sample and a test stimulus, separated by a delay period. Furthermore, we offer the mechanism by which the synaptic structures of the neural circuits involved in the DMS task are generated via the task training. The results provide a unified view of how WM maintenance is linked to its manipulation.
... Secondly, we also found that the FC between the left lateral OFC and left superior medial frontal cortex is negatively correlated with conscientiousness and positively correlated with crystallized cognition. The OFC in the ventral surface of the prefrontal lobe is involved in the cognitive process of sensory integration, emotion processing, and decision-making [76][77][78]. And the superior medial frontal cortex which is part of SFG is correlated with inhibitory control ability and other cognitive function [67,79]. ...
Article
Full-text available
Perceived stress impairs cognitive function across the adult lifespan, but the extent to which cognition decline is variable across individuals. Individual differences in the stress response are described as personality traits. Substantial individual differences in the magnitude of cognitive impairment that is induced by short-term perceived stress are poorly understood. The present study tested the hypothesis that the relationship between short-term perceived stress and different aspects of cognition is mediated by personality traits. The study included 1066 participants with behavior and neuroimaging data from the Human Connectome Project after excluding individuals with missing variables. In the result, the parallel multiple mediation model demonstrated that the influence of perceived stress on the total and crystalized cognition is mainly mediated by neuroticism (indirect effect = −0.04, p < 0.05) and conscientiousness (indirect effect = 0.05, p < 0.05) in adults. Cortical thickness value (n = 1066) of the right superior frontal gyrus (SFG) showed not only positive correlations with short-term perceived stress and neuroticism, but negative associations with cognition. The chain mediation model found that the right SFG and neuroticism play a small but significant chain mediating effect between stress and total cognition. The strength of the resting-state functional connectivity (n = 968) between the left orbitofrontal cortex versus the left superior medial frontal cortex was positively correlated with crystallized cognition and negatively associated with conscientiousness. These results extend previous findings by the impacts of short-term perceived stress on cognitive function is mediated by neuroticism and the right SFG was the underlying neural mechanism.
... The effects of CHO mouth rinses on the attenuation of a decrease in prolonged exercise performance is speculated to involve neural mechanisms [6]. In response to oral CHO, brain regions within the dorsolateral prefrontal cortex, anterior cingulate cortex, and caudate nucleus, which form part of the striatum, are activated [4]; the orbitofrontal cortex, which is part of the reward value of taste, is also involved [30,31]. Furthermore, CHO mouth rinses increase the executive function and self-control in the brain [32][33][34]. ...
Article
Full-text available
Mouth rinsing with a carbohydrate (CHO) solution has emerged as a sports nutrition strategy to increase endurance performance. This study aimed to clarify the effects of two forms of CHO sensing in the mouth (i.e., CHO mouth rinse (CMR) and CHO mouth spray (CMS)) on exercise performance during prolonged exercise, including ultra-high intensity intermittent exercise over time. We conducted the following experimental trials: (1) 6% glucose solution (G), (2) 6% CMR, (3) 6% CMS, and (4) water (WAT). These trials were conducted at least 1 week apart in a randomized crossover design. Eight male college students performed constant-load exercise for 60 min (intensity 40% VO2peak), four sets of the Wingate test (three 30 s Wingate tests with a 4 min recovery between each test), and a constant-load exercise for 30 min (intensity 40% VO2peak). The mean exercise power output (Watt), ratings of perceived exertion, and blood glucose levels were measured. We found that the mean power values of the CMR and CMS in the third and fourth sets was significantly higher than that of WAT (p < 0.05), and that the G trial did not show a significant difference from any other trial. Thus, when compared to G or WAT, CMR and CMS can help improve endurance exercise performance.
... • The orbitofrontal cortex is crucial for stimulus-reinforcement learning (Edmund T. Rolls, 1990) • development of personal moral-based knowledge based on the processing of rewards and punishments (Dolan, 1999) • Involves stimulus-stimulus learning, as would be consistent with the neurophysiology of the primate orbitofrontal cortex in which sensory-reinforcement association learning is represented but motor responses are not (E. T. Rolls, 2000) ...
Book
This book summarises and organises localised neuropsychological functions of frontal lobes in an easy-to-understand manner for visual learners. We have laced the book with tables, graphics, and other media to help add to the learning process. At the end of the book, you face a series of questions to help you test your learning. We cite reliable sources as we describe the anatomy, functions, deficits and assessment of the various regions of the human frontal lobes.
... During valuation, decision-makers attribute subjective value to the choice options they consider, thereby forming a neural representation of value. Converging evidence from neurophysiological and lesion studies, some of which date back to the 1980s (for overviews, see Montague and Berns, 2002;Rolls, 2000), as well as from ensuing brain imaging studies (Bartra et al., 2013;Clithero and Rangel, 2014) suggest frontal brain regions, particularly the ventromedial prefrontal cortex (vmPFC), to show an activity profile that matches the idea of a representation of subjective value. vmPFC seems to construct and integrate value signals (Bault et al., 2019;Chib et al., 2009;Vaidya and Fellows, 2020) and contribute to the comparison between value-based choice options (Boorman et al., 2009;Rushworth et al., 2011). ...
Article
Full-text available
Value-based decisions depend on different forms of memory. However, the respective roles of memory and valuation processes that give rise to these decisions are often vaguely described and have rarely been investigated jointly. In this review article, we address the problem of memory-based decision making from a neuroeconomic perspective. We first describe the neural and cognitive processes involved in decisions requiring memory processes, with a focus on episodic memory. Based on the results of a systematic research program, we then spotlight the phenomenon of the memory bias, a general preference for choice options that can be retrieved from episodic memory more successfully. Our findings indicate that failed memory recall biases neural valuation processes as indicated by altered effective connectivity between the hippocampus and ventromedial prefrontal cortex. This bias can be attributed to meta-cognitive beliefs about the relationship between subjective value and memory as well as to uncertainty aversion. After summarizing the findings, we outline potential future research endeavors to integrate the two research traditions of memory and decision making.
... In line with the observations from the separate dataset analysis, the right anterior insula extending into the adjacent inferior frontal gyrus and the left fusiform gyrus specifically exhibited convergent engagement during core and social disgust processing. Together with the anterior insula, the inferior frontal cortex plays an important role in general emotional processes such as evaluation of biological significant stimuli (Rolls, 2000a(Rolls, , 2004, interoception (Critchley et al., 2004), multimodal representation emotion salient stimuli (Yamasaki et al., 2002), and emotion recognition (Sprengelmeyer et al., 1998), while the fusiform gyrus plays a role in higher order visual processing (Fusar-Poli et al., 2009b) and emotional reactivity towards negative and threatening stimuli (Kirby and Robinson, 2017;Tao et al., 2021). Initial original studies have begun to examine the shared neural substrates for core and social disgust. ...
Article
Disgust represents a multifaceted defensive-avoidance response. On the behavioral level, the response includes withdrawal and a disgust-specific facial expression. While both serve the avoidance of pathogens, the latter additionally transmits social-communicative information. Given that common and distinct brain representation of the primary defensive-avoidance response (core disgust) and encoding of the social-communicative signal (social disgust) remain debated, we employed neuroimaging meta-analyses to (1) determine brain systems generally engaged in disgust processing, and (2) segregate common and distinct brain systems for core and social disgust. Disgust processing, in general, engaged a bilateral network encompassing the insula, amygdala, occipital and prefrontal regions. Core disgust evoked stronger reactivity in left-lateralized threat detection and defensive response network including amygdala, occipital and frontal regions, while social disgust engaged a right-lateralized superior temporal-frontal network engaged in social cognition. Anterior insula, inferior frontal and fusiform regions were commonly engaged during core and social disgust, suggesting a shared neurofunctional basis. We demonstrate a common and distinct neural basis of primary disgust responses and encoding of associated social-communicative signals.
... L'OFC est une région importante qui confère des informations relatives à la valeur récompensante de stimuli gustatifs (Rolls et al., 1989), olfactifs et visuels (Critchley and Rolls, 1996;Rolls, 2000). ...
Thesis
Les produits du tabac sont hautement addictifs et leur abus est un problème majeur de santé publique. Chez les humains, cette addiction met en jeu une expérience consommatoire orale avec des composantes sensorielles gustatives et olfactives. De nos jours, le rôle de ces composantes est amplifié avec l’utilisation accrue des produits du tabac non-brûlé, mais aussi les cigarettes électroniques, où la nicotine est associée à des additifs incluant flaveurs et sucres. L’impact des additifs sur le comportement de consommation du tabac doit donc être évalué. Dans ce travail de recherche, notre intérêt se porte sur la nicotine orale et l’interaction bidirectionnelle avec les flaveurs associées. Nous questionnons notamment les propriétés de renforcement secondaire, les effets des arômes sur la palatabilité de la nicotine et son encodage affectif. Dans un premier chapitre, nous avons investigué les propriétés irritantes de la nicotine dans un modèle d’auto-administration orale de nicotine diluée dans de la saccharine chez des souris génétiquement modifiées (knockout) pour le thermorécepteur TRPV1 (Transient receptor potential vanilloid 1), impliqué dans l’échauffement lié au tabagisme et qui a la particularité d’être sensibilisé par la nicotine. Nous mettons en évidence que l’absence de ce récepteur promeut la consommation de nicotine par diminution de son aversion orale. Il n’a cependant pas un rôle spécifique dans les mécanismes de motivation et de rechute. Il a été montré que les stimuli sensoriels non-pharmacologiques deviennent plus salients quand ils sont associés à la nicotine. Ainsi, nous étudions dans un deuxième chapitre, le renforcement secondaire putatif des stimuli oraux par la nicotine. Nous mettons en évidence la nécessité d’association orale de la nicotine à des additifs masquant son goût amer, afin de permettre sa consommation volontaire et la modélisation des différents stades du processus addictif. Ce processus se montre sensible aux stimuli dans la consommation et la rechute, mais insensible aux challenges pharmacologiques malgré l’absorption de nicotine mesurée par la présence de cotinine plasmatique. Les solutions de nicotine à fortes concentrations révèlent des propriétés aversives et réduisent la consommation volontaire. Bien que nous ne montrions pas le renforcement des propriétés incitatives de la vanille par la nicotine, de façon surprenante nous montrons que l’arôme seul peut renforcer le comportement d’auto-administration. Enfin, du fait de l’importance des effets sensoriels oraux dans la consommation de nicotine, nous avons étudié ses propriétés de palatabilité. Les tests de réactivité gustative montrent bien l’aversion gustative pour la nicotine seule et l’amélioration de la palatabilité par l’ajout d’additif aromatique. Ce changement de la palatabilité ne s’est néanmoins pas traduit par des changements du codage neuronal mesuré par le marquage de la protéine c-Fos dans les structures contribuant à l’expression de la valence positive ou négative, notamment le noyau accumbens, le cortex insulaire gustatif, le noyau basolatéral de l’amygdale, l’habenula et la noyau paraventriculaire du thalamus. En revanche, la nicotine, aromatisée ou non, a augmenté l’activation neuronale dans toutes ces structures. L’ensemble de ces résultats met en lumière cette problématique d’association de la nicotine aux additifs pouvant moduler sa perception sensorielle et promouvoir par la suite sa consommation. L’attractivité des nouveaux produits du tabac et leur potentiel d’abus est une question authentique et un problème de santé publique dont l’étude et la régulation sont urgentes.
... Brain activity in the frontal and parietal regions related to the acceptance of gambles is consistent with previous results that brain activity increases in the frontal and parietal regions when expectations for rewards are high (Fig. S2C) ( Hare et al., 2008 ;Rolls, 2000 ;Tom et al., 2007 ). The frontal and parietal activations related to the increase in probability can also be explained by the higher expectations for rewards. ...
Article
Full-text available
In real life, humans make decisions by taking into account multiple independent factors, such as delay and probability. Cognitive psychology suggests that cognitive control mechanisms play a key role when facing such complex task conditions. However, in value-based decision-making, it still remains unclear to what extent cognitive control mechanisms become essential when the task condition is complex. In this study, we investigated decision-making behaviors and underlying neural mechanisms using a multifactor gambling task where participants simultaneously considered probability and delay. Decision-making behavior in the multifactor task was modulated by both probability and delay. The behavioral effect of probability was stronger than delay, consistent with previous studies. Furthermore, in a subset of conditions that recruited fronto-parietal activations, reaction times were paradoxically elongated despite lower probabilistic uncertainty. Notably, such a reaction time elongation did not occur in control tasks involving single factors. Meta-analysis of brain activations suggested an interpretation that the paradoxical increase of reaction time may be associated with strategy switching. Consistent with this interpretation, logistic regression analysis of the behavioral data suggested a presence of multiple decision strategies. Taken together, we found that a novel complex value-based decision-making task cause prominent activations in fronto-parietal cortex. Furthermore, we propose that these activations can be interpreted as recruitment of cognitive control system in complex situations.
... 作为应用 rTMS 或伪刺激(SHAM)的靶点,因为它在许多高阶脑功能中起关键 作用,例如注意 [124,125] ,工作记忆 [126][127][128][129] ,认知控制 [130] ,以及决策 [131][132][133] [138] ,情绪调节 [139,140] ,冲 动控制 [124,141] 和决策 [94,[142][143][144][145][146] ...
Thesis
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熵表示系统不规则性和信息处理能力。人脑是世界上最复杂的系统之一,使用脑熵(BEN)来评估大脑复杂性可能提供一些物理特征来增加我们对脑活动的理解。在过去使用脑电数据已经对BEN进行过评估,但是由于缺乏足够的空间分辨率,最近我们使用样本熵提出了基于功能磁共振的BEN测量方法。并且最近的BEN研究已经确定了正常BEN分布模式,另外也有一些研究发现了在衰老和脑疾病上的BEN变化,这些先期研究清楚地表明了BEN很可能会成为一个新兴的生物标记。正因为它相对比较新颖,在临床或基础的认知神经科学界,BEN的接受度还相对较低。究其原因,一是BEN与现有广为人知的方法之间的关系不清晰,二是BEN是否可逆,是否能反映神经调控或治疗效果不得而知。围绕BEN这个前沿课题,本论文课题主要解决以上两个关键问题。在第一部分我们研究BEN与脑血流(CBF),比率低频振幅(fALFF)之间的关系,为BEN作为测量静息态脑活动的一个新指标提供更多证据;在第二部分,我们研究左侧背外侧前额叶(DLPFC)高频重复经颅磁刺激(rTMS)对BEN的影响,来验证BEN对神经调控的敏感性和作为潜在地生物标记提供证据。第一部分静息态BEN与CBF,fALFF之间的关系熵是人脑的基本特征。使用基于fMRI的BEN映射,在正常脑和神经精神疾病中越来越多地发现了有趣的发现。由于BEN仍然相对较新,一个经常被提出的问题是,与其他更成熟的大脑活动指标相比,这一衡量标准可以告诉有多少新信息。该研究旨在通过检查BEN和两种广泛使用的静息状态脑状态测量方法CBF,fALFF之间的关系来解决这个问题。从一个大样本被试中获得的fMRI数据用于计算三个指标;通过皮尔逊相关分析在每个体素上评估模态间关联。结果表明在眶额皮层(OFC)和后部颞下回(ITC)区域BEN-CBF,BEN-fALFF有中等到强的正相关关系;在视觉皮层(VC),纹状体,前部ITC,运动网络,楔前叶和外侧顶叶皮层中发现BEN-fALFF有着强的负相关关系。在内侧眶额皮层(MOFC),内侧前额叶(MPFC),左侧角回和左前额叶中发现了CBF-fALFF有强的负相关关系。三种测量方式之间的相关关系也存在着显著的性别差异。我们的数据清楚地表明,BEN提供了CBF和fALFF无法揭示的独特信息。第二部分rTMS对BEN的影响最近的研究已经确定在正常大脑中显示出有趣的BEN分布模式及其由于衰老和脑部疾病引起的变化。但是一个具有重要科学和临床重要性的问题,使用非侵入性神经调节是否可以调节BEN仍然是未知的。本研究的目的是使用高频rTMS来解决这个开放性问题。应用20Hz rTMS或SHAM(对照)刺激之前和之后获得的静息状态fMRI计算BEN。与SHAM相比,20Hz rTMS减少了内侧眶额皮层和膝下扣带回(MOFC/sgACC)中的BEN,表明其中信息处理减少,这可能是由于左侧DLPFC rTMS增强的自上而下调节。左侧DLPFC(靶点)与大脑其他部位之间的功能连接性(FC)未观察到显著变化,表明rTMS可能不会影响FC,尽管它可能使用FC来转移其效果或及时性信息。我们的数据证明rTMS可以调节BEN,BEN可用于监测rTMS效应。
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Chapter
Since the paper of Heimer and Wilson (1975), great interest has focussed on the anatomy of the ventral striatum, which includes the nucleus accumbens, the olfactory tubercle (or anterior perforated substance of primates), and the islands of Calleja. They showed that the ventral striatum receives inputs from limbic structures such as the amygdala and hippocampus, and projects to the ventral pallidum. The ventral pallidum may then influence output regions by the subthalamic nucleus / globus pallidus / ventral thalamus / premotor cortex route, or via the mediodorsal nucleus of the thalamus / prefrontal cortex route (Heimer et al, 1982). The ventral striatum may thus be for limbic structures what the neostriatum is for neocortical structures, that is a route for limbic structures to influence output regions. The dopamine pathways are at a critical position in these systems, for the nigro-striatal pathway projects to the neostriatum, and the mesolimbic dopamine pathway projects to the ventral striatum (Ungerstedt, 1971). Indeed, Nauta and Domesick (1978) have provided evidence that the ventral striatum also provides a route for limbic information to influence the neostriatum, via the projections of the ventral striatum to the substantia nigra (A9), and thus via the dopamine pathways to the neostriatum. This pattern of connections of the ventral striatum appears to occur not only in the rat (Heimer and Wilson, 1975; Newman and Winans, 1980a,b), but also in the primate (Hemphill et al, 1981). In addition, it is now clear that the olfactory tubercle is in the anterior perforated substance in the primate (Heimer et al, 1977), and that while a small part of it related to the olfactory tract does receive olfactory projections, a much larger part of it receives a strong projection from the inferior temporal visual cortex (Van Hoesen et al, 1976, 1981), and could thus provide a link from temporal lobe association cortex to output regions.