Rolls has developed a framework for understanding brain mechanisms of
emotion in primates and humans based on mechanisms that represent
reward and punishment value in the orbitofrontal cortex but not at
earlier stages of cortical processing, and in which the orbitofrontal
cortex largely overshadows the amygdala. Rolls and colleagues
discovered reward and punishment value, and non-reward, neurons in the
primate orbitofrontal cortex; and discovered how taste and olfactory
processing in primates occurs to produce reward value representations
of the sight, smell, taste and fat texture of food in the orbitofrontal
cortex that is importnat in understanding appetite and obesity. These
discoveries are complemented by fMRI in humans, by investigation
of emotional disorders that follow brain damage in humans (641), and by an
approach based on these foundations to understanding depression in
humans. Key summary descriptions are in B14, B11, 634, 626, 579 and 558. A summary aimed to help the general reader is in B13.
theory of emotion, and pleasure, and reward; and the principles of
implementation in the brain (B5,
B11, B13, B14, B15, 273, 520,
148, 364, 428, 509, 526, 531, 533,
534, 542, 552, 579).
A key principle in primates
including humans is that reward value and emotional valence are
represented in the orbitofrontal cortex (and amygdala), whereas before
that, the representations are about objects and stimuli independently
of value, in the inferior temporal visual cortex, the primary taste
cortex in the insula, and in the olfactory cortex (B11, B13, B14, B15). This provides for the separation of emotion from perception.
In this framework, the dopamine
neurons are seen as receiving their information from brain regions such
as the orbitofrontal cortex, via the ventral striatum and habenula (572, B11, B13, B14).
Further, orbitofrontal cortex neurons encode reward value and hence
emotion, independently of goal-related actions. The orbitofrontal
cortex provides reward-related information to the cingulate cortex for
action-outcome learning, and to the basal ganglia for habit-based
responses (B11, B13, B14, 579, 606).
theory of motivation
hypothalamic neurons with visual and taste responses to food. These
only respond when hunger is present, so encode the reward value of
food. (25, 26. 27,
37, 57, B7,
satiety, discovered by recordings from lateral hypothalamic neurons
(46, 47, 55,
57, 59, 68, 69, 82, 89, 104, 234).
of taste, olfactory, flavour, and visual sensory-specific satiety in
orbitofrontal cortex (124, 285).
for brain-stimulation reward: activation of neurons normally activated
natural rewards (12, 48, B1,
primary taste cortex (119, 120, 437, 552),
the primary olfactory
and the inferior
temporal visual cortex (32) encode information about the
identity and intensity
of the taste, odour or sight of objects, but not about their reward value (B11, B15).
secondary taste cortex (in the orbitofrontal cortex, including lateral
medial parts) (124, 141,
tertiary taste cortex (in the anterior cingulate cortex) (443,
convergence of taste, olfactory and visual inputs onto single neurons
orbitofrontal cortex to produce flavour (189,
212). Age differences in this flavor reward system (544).
first cortical region in which information about reward value is made
in the representation in primates including humans is the orbitofrontal cortex (124, 291,
495, 579, B11, B14, B15), and a
second is the anterior
cingulate cortex (443,
468, 495, B14, B15).
role of sensory-specific satiety, variety in the food available, and
cognitive and attentional control reward representations in the
cortex in appetite control and obesity, with implications for the prevention and control of obesity (416,
487, 519, 542, B11, 558, 634, 638).
regions where activity is associated with the subjective conscious
feeling of pleasure,
including the orbitofrontal cortex and anterior cingulate cortex (334,
434, 462, 495, 542, 544, B11, B13, B14).
orbitofrontal cortex is involved in one-trial rule-based visual stimulus-reward
and contains negative reward prediction error neurons (79,
337, 579, 627,
B11, B13, B14).
The lateral orbitofrontal cortex is activated during reward
reversal and behavioural inhibition, when behaviour must be changed (337, 575, 627, B13, B14, B15, 626).
texture, including viscosity, astringency, and fat texture, and oral
temperature, are represented in the primary taste cortex, the
cortex, and the amygdala (210, 346,
376, 425, 499,
528, 542, 593, 610).
sensed by its texture in the mouth (269,
363, 472, 475, 499).
The fat sensing is by the coefficient of sliding friction, not by
viscosity or by free fatty acids which are separately represented (593).This
has important implications for the development of foods with a similar texture,
energy content (593, 610).
control of reward value and emotion by cognition and attention (381,
488, 520, 530, B11).
between the taste of monosodium glutamate and consonant vegetable
produce the rich delicious flavour umami (158,
representation of economic value in the orbitofrontal cortex, with
regions responding to monetary gains and losses (288,
and both absolute
and relative value represented (467)
(see 495, B11, B14), with implications for economics (600).
decision-making in the ventromedial prefrontal cortex / medial prefrontal cortex area 10, and the
of confidence about decisions (452,
454, 481, 486, 489, 495, 513, B9, B11, B14, B15).
principles of operation of the orbitofrontal cortex in humans and other
478, 494, 495, 531, 579, 608, B7, B11, B13, B14). The connections of the orbitofrontal cortex that helps to implement its functions (190, 608, 620).
neurons in the amygdala (38, 91, 97), inferior temporal visual cortex (38A,
96, 162), and orbitofrontal cortex (397)
(see 412, 451, 501, 578, B11, B12, B14).
expression selective neurons in the cortex in the superior temporal
126) and orbitofrontal cortex (397). Reduced functional and effective connectivity in this region in autism (541, 570, 609).
in the rapid rule-based reversal of associations between stimuli and reward value
patients with selective lesions of the orbitofrontal cortex and related
their relation to emotional changes (188,
354). Also, impairments in
These discoveries were
inspired by the discoveries
on neuronal activity in the orbitofrontal cortex, and are relevant to
the changes in patients with frontal lobe damage and in patients with
borderline personality disorder (B14).
A non-reward attractor theory of depression (559, 572, B13)
supported by altered connectivity and activations of the orbitofrontal
cortex in depression (564, 579, 583, 588
, 591, 592, 596, 623, 626, B14, B15)
, and a model of the computation of non-reward in
the orbitofrontal cortex (562). An introduction to the theory is available as a lecture.
roles of the cingulate cortex in emotion, action, and memory, and their
disorders, together with the concept that there is no single limbic
system (B11, 531, 588, 596, 606, 608).
A model for action-outcome learning in which action-related information
reaches the posterior cingulate cortex from the parietal cortex, is
associated with reward outcome information reaching the anterior
cingulate cortex from the orbitofrontal cortex, with outputs from the
midcingulate cortex reaching the premotor cortex (606)
Consistent with this, sensation-seeking can be predicted from the
connectivity between the reward-related medial orbitofrontal cortex and
the anterior cingulate cortex (619).
ganglia: each part of the striatum contains neurons that respond to
received from the cortical areas that project into each striatal
this information is brought together by the architecture of the
globus pallidus, and substantia nigra in a way that appears to provide
selection of one behavioural output as a result of competition between
inhibitory neurons in these parts of the basal ganglia (80, 84, 147, 174, 181, B7,
of Granger causality and their application to functional neuroimaging:
componential Granger causality (which allows the effects of
interactions to be
measured); and Granger causality with signal-dependent noise (with
and colleagues) (505, 530). The use of effective (directed) connectivity in large-scale analyses of the neural bases of depression (583), schizophrenia (602), and autism (609).
relation to addiction, the medial orbitofrontal cortex reward system
has high functional connectivity in those who tend to drink alcohol and
who are sensation-seekers and are impulsive, and the lateral
orbitofrontal cortex non-reward system has low functional connectivity
in those who tend to smoke and are impulsive (599). The medial orbitofrontal cortex is also activated by amphetamine (367), and has high functional connectivity in users of arecoline (betel quid) (617).
Reward systems and aesthetics
(B10, B11, 509,
532, 556, 574).