The orbitofrontal cortex: Neuronal activity in the behaving monkey
Abstract
Single unit recording of neurons in the orbitofrontal cortex of the alert rhesus monkey was used to investigate responses to sensory stimulation. 32.4% of the neurons had visual responses that had typical latencies of 100-200 ms, and 9.4% responded to gustatory inputs. Most neurons were selective, in that they responded consistently to some stimuli such as foods or aversive objects, but not to others. In a number of cases the neurons responded selectively to particular foods or aversive stimuli. However, this high selectivity could not be explained by simple sensory features of the stimulus, since the responses of some neurons could be readily reversed if the meaning of the stimulus (i.e. whether it was food or aversive) was changed, even though its physical appearance remained identical. Further, some bimodal neurons received convergent visual and gustatory inputs, with matching selectivity for the same stimulus in both modalities, again suggesting that an explanation in terms of simple sensory features is inadequate. Neurons were also studied during the performance of tasks known to be disrupted by orbitofrontal lesions, including a go/no go visual discrimination task and its reversal. 8.6% of neurons had differential responses to the two discriminative stimuli in the task, one of which indicated that reward was available and the other saline. Reversing the meaning of the two stimuli showed that whereas some differential units were closely linked to the sensory features of the stimuli, and some to their behavioural significance, others were conditional, in that they would only respond if a particular stimulus was present, and if it was the one being currently rewarded. Other neurons had activity related to the outcome of the animal's response, with some indicating that reinforcement had been received and others, that an error had been made and that a reversal was required. Thus, neurons in the orbitofrontal cortex possess highly coded information about which stimuli are present, as well as information about the consequences of the animal's own responses. It is suggested that together they may constitute a neuronal mechanism for determining whether particular visual stimuli continue to be associated with reinforcement, as well as providing for the modification of the animal's behavioural responses to such stimuli when those responses are no longer appropriate.
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In visual discrimination reversal experiments, neurons in the macaque OFC reverse the visual stimulus in as little as one trial when the reward versus punishment taste received as an outcome for the choice reverses.
“In visual discrimination reversal experiments, neurons in the macaque OFC reverse the visual stimulus in as little as one trial when the reward versus punishment taste received as an outcome for the choice reverses (Thorpe et al., 1983; Rolls et al., 1996).”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Thorpe et al., 1983
The macaque OFC contains neurons that reflect face expression and face identity, social categories such as young faces, and position in the social hierarchy.
“The macaque OFC contains neurons that reflect face expression and face identity (both necessary to decode value and important in social behaviour) (Thorpe et al., 1983; Rolls et al., 2006), and also social categories such as young faces (Barat et al., 2018) and position in the social hierarchy (Munuera et al., 2018).”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Thorpe et al., 1983
The macaque OFC has neurons that respond when an expected reward is not received (non-reward neurons).
“The macaque OFC has neurons that respond when an expected reward is not received (Thorpe et al., 1983), and these have been termed non-reward neurons (Rolls, 2014, 2019c) (see example in Fig. 4C).”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Thorpe et al., 1983
Non-reward and punishment are represented by different neurons in the OFC.
“These neurons do not respond to expected punishers [e.g. the discriminative stimulus for saline in Fig. 4C; (Thorpe et al., 1983)], but other neurons do respond to expected punishers (Rolls et al., 1996), showing that non-reward and punishment are represented by different neurons in the OFC.”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Thorpe et al., 1983
The finding of non-reward neurons is robust: 18/494 (3.6%) of neurons in the original study responded to non-reward, 10/140 (7.1%) in a complementary study, and an fMRI study showed macaque lateral OFC activation when expected reward was not obtained during reversal.
“The finding of non-reward neurons is robust, in that 18/494 (3.6%) of the neurons in the original study responded to non-reward (Thorpe et al., 1983), consistent results were found in different tasks in a complementary study (10/140 non-reward neurons in the OFC or 7.1%) (Rosenkilde et al., 1981), and an fMRI study has shown that the macaque lateral OFC is activated when an expected reward is not”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Thorpe et al., 1983
The primate OFC specializes in reward (and punishment and non-reward) value representations, but not in interfacing these value representations to actions or to responses.
“The primate OFC, in contrast, appears to specialize in reward (and of course punishment and non-reward) value representations, but not in interfacing these value representations to actions [which occurs in the primate cingulate cortex (Rolls, 2019b2021a)] or to responses (which occurs in the striatum and other parts of the basal ganglia), for actions and responses are poorly if at all represented”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Thorpe et al., 1983
Non-reward neurons in the lateral OFC can maintain their activity for at least many seconds.
“Because non-reward neurons in the lateral OFC can maintain their activity for at least many seconds (Fig. 4) (Thorpe et al., 1983), and because this persistent activity is needed to ensure that after non-reward, the behaviour changes even if the same stimuli are not received for some time, the theory is that there is a non-reward attractor network in the lateral OFC, and that this is more”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Thorpe et al., 1983
Actions and responses are poorly if at all represented in the primate OFC.
“The primate OFC, in contrast, appears to specialize in reward (and of course punishment and non-reward) value representations, but not in interfacing these value representations to actions [which occurs in the primate cingulate cortex (Rolls, 2019b2021a)] or to responses (which occurs in the striatum and other parts of the basal ganglia), for actions and responses are poorly if at all represented”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Thorpe et al., 1983
Rodent reward reversal learning does not so far appear to be of the same powerful type as the rule-based system present in primates, which allows switching to a different stimulus even previously associated with punishment when no reward is received when it was expected by a behavioural choice on a single trial.
“Fifth, although reward reversal learning is studied in rodents (Hervig et al., 2020), it does not so far appear to be of the same powerful type as the rule-based system present in primates, which allows switching to a different stimulus even previously associated with punishment when no reward is received when it was expected by a behavioural choice on a single trial (Thorpe et al., 1983; Rolls et”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Thorpe et al., 1983
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- Authors
- Thorpe, S. J., Rolls, E. T., & Maddison, S.
- Affiliations
- University of Oxford (GB)
- Venue
- Experimental Brain Research
- Published
- 1983-01
- Volume
- 49
- Issue
- 1
- Pages
- 93-115
- ISSN
- 0014-4819 (ISSN-L)
- 1432-1106
- OpenAlex
- W2085755382
- Cited by
- 836
- References
- 52
- Citations by year
- 2026: 6 · 2025: 17 · 2024: 17 · 2023: 5 · 2022: 15 · 2021: 22 · 2020: 17 · 2019: 19 · 2018: 18 · 2017: 25 · 2016: 28 · 2015: 24 · 2014: 20 · 2013: 24 · 2012: 21
- FWCI
- 8.74
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Experimental Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- orbitofrontal cortex, rhesus monkeys, single-unit recording, bimodal neurons, go/no-go task, reversal learning, error signal, reinforcement, stimulus meaning
- MeSH terms
- Animals, Appetitive Behavior, Association Learning, Avoidance Learning, Conditioning, Operant, Discrimination Learning, Evoked Potentials, Visual, Extinction, Psychological, Frontal Lobe, Macaca mulatta, Male, Neurons, Reaction Time, Reinforcement Schedule, Reversal Learning, Taste, Visual Perception
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