Oxford Centre for Computational Neuroscience

Professor Edmund T. Rolls

Discoveries on emotion, reward, pleasure, motivation, decision-making, taste, olfaction, and appetite including implications for the control of food intake and obesity

Emotion and Decision-Making Explained


The Noisy Brain

Memory, Attention, and Decision-Making

Overview: 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.

A theory of emotion, and pleasure, and reward; and the principles of their 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).

A theory of motivation (557).


Lateral hypothalamic neurons with visual and taste responses to food. These neurons only respond when hunger is present, so encode the reward value of food. (25, 26. 27, 37, 57, B7, B11).


Sensory-specific satiety, discovered by recordings from lateral hypothalamic neurons (46, 47, 55, 57, 59, 68, 69, 82, 89, 104, 234).


Implementation of taste, olfactory, flavour, and visual sensory-specific satiety in the orbitofrontal cortex (124, 285).


A basis for brain-stimulation reward: activation of neurons normally activated by natural rewards (12, 48, B1, B7).


The primary taste cortex (119, 120, 437, 552), the primary olfactory cortex (442), 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).


The secondary taste cortex (in the orbitofrontal cortex, including lateral and medial parts) (124, 141, 190, 382).


The tertiary taste cortex (in the anterior cingulate cortex) (443, 468).


Multimodal convergence of taste, olfactory and visual inputs onto single neurons in the orbitofrontal cortex to produce flavour (189, 366, 382) using associative learning (211, 212). Age differences in this flavor reward system (544).


The first cortical region in which information about reward value is made explicit in the representation in primates including humans is the orbitofrontal cortex (124, 291, 322, 333, 367, 441, 495, 579, B11, B14, B15), and a second is the anterior cingulate cortex (443, 468, 495, B14, B15).


The role of sensory-specific satiety, variety in the food available, and top-down cognitive and attentional control reward representations in the orbitofrontal cortex in appetite control and obesity, with implications for the prevention and control of obesity (416, 420, 426, 484, 487, 519, 542, B11, 558, 634, 638).


Brain regions where activity is associated with the subjective conscious feeling of pleasure, including the orbitofrontal cortex and anterior cingulate cortex (334, 335, 338, 434, 462, 495, 542, 544, B11, B13, B14).


The orbitofrontal cortex is involved in one-trial rule-based visual stimulus-reward learning, 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).


Oral texture, including viscosity, astringency, and fat texture, and oral temperature, are represented in the primary taste cortex, the orbitofrontal cortex, and the amygdala (210, 346, 352, 361, 363, 376, 425, 499, 528, 542, 593, 610).


Fat is sensed by its texture in the mouth (269, 336, 352, 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, but low energy content (593, 610).


Top-down control of reward value and emotion by cognition and attention (381, 434, 437, 440, 442, 480, 488, 520, 530, B11).


Synergism between the taste of monosodium glutamate and consonant vegetable odours to produce the rich delicious flavour umami (158, 243, 279, 330, 417, 469).


The representation of economic value in the orbitofrontal cortex, with different regions responding to monetary gains and losses (288, 424), and both absolute and relative value represented (467) (see 495, B11, B14), with implications for economics (600).


Reward-related decision-making in the ventromedial prefrontal cortex / medial prefrontal cortex area 10, and the representation of confidence about decisions (452, 454, 481, 486, 489, 495, 513, B9, B11, B14, B15).


The principles of operation of the orbitofrontal cortex in humans and other primates (270, 356, 389, 357, 435, 452, 474, 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).

Face-selective neurons in the amygdala (38, 91, 97), inferior temporal visual cortex (38A, 73, 91, 96, 162), and orbitofrontal cortex (397) (see 412, 451501, 578, B11, B12, B14)


Face expression selective neurons in the cortex in the superior temporal sulcus (114, 126) and orbitofrontal cortex (397). Reduced functional and effective connectivity in this region in autism (541, 570, 609).


Impairments in the rapid rule-based reversal of associations between stimuli and reward value in patients with selective lesions of the orbitofrontal cortex and related areas and their relation to emotional changes (188, 203, 331, 354). Also, impairments in impulsivity (353, 362, 394). These discoveries were inspired by the discoveries on neuronal activity in the orbitofrontal cortex, and are relevant to understanding 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.

The 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).

Basal ganglia: each part of the striatum contains neurons that respond to information received from the cortical areas that project into each striatal region, but this information is brought together by the architecture of the striatum, globus pallidus, and substantia nigra in a way that appears to provide for selection of one behavioural output as a result of competition between mutually inhibitory neurons in these parts of the basal ganglia (80, 84, 147, 174, 181, B7, B11).


Extensions 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 J.Feng, T.Ge 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).

In 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).