Orbitofrontal cortex neurons: role in olfactory and visual association learning.

1. The orbitofrontal cortex is implicated in the rapid learning of new associations between visual stimuli and primary reinforcers such as taste. It is also the site of convergence of information from olfactory, gustatory, and visual modalities. To investigate the neuronal mechanisms underlying the formation of odor-taste associations, we made recordings from olfactory neurons in the orbitofrontal cortex during the performance of an olfactory discrimination task and its reversal in macaques. 2. It was found that 68% of odor-responsive neurons modified their responses after the changes in the taste reward associations of the odorants. Full reversal of the neuronal responses was seen in 25% of these neurons. Extinction of the differential neuronal responses after task reversal was seen in 43% of these neurons. 3. For comparison, visually responsive orbitofrontal neurons were tested during reversal of a visual discrimination task. Seventy-one percent of these visual cells showed rapid full reversal of the visual stimulus to which they responded, when the association of the visual with taste was reversed in the reversal task. 4. These demonstrate that of many orbitofrontal cortex olfactory neurons on the taste with which the odor is associated. 5. This modification is likely to be important for setting the motivational value of olfactory for feeding and other rewarded behavior. However, it is less complete, and much slower, than the modifications found or orbit frontal visual during visual-taste reversal. This relative inflexibility of olfactory responses is consistent with the need for some stability is odor-taste associations to facilitate the formation and perception of flavors.

[1]  E. Rolls,et al.  Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[2]  E. T. Rolls,et al.  Effects of satiety on self-stimulation of the orbitofrontal cortex in the rhesus monkey , 1979, Neuroscience Letters.

[3]  E. Rolls,et al.  Hunger Modulates the Responses to Gustatory Stimuli of Single Neurons in the Caudolateral Orbitofrontal Cortex of the Macaque Monkey , 1989, The European journal of neuroscience.

[4]  H. Eichenbaum,et al.  Odor-guided learning and memory in rats: is it ‘special’? , 1993, Trends in Neurosciences.

[5]  E. Rolls,et al.  Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex. , 1996, Journal of neurophysiology.

[6]  D. R. Snyder,et al.  Effects of orbital frontal lesions on aversive and aggressive behaviors in rhesus monkeys. , 1970, Journal of comparative and physiological psychology.

[7]  M. Mishkin,et al.  Limbic lesions and the problem of stimulus--reinforcement associations. , 1972, Experimental neurology.

[8]  B. Slotnick The enigma of olfactory learning , 1993, Trends in Neurosciences.

[9]  H Eichenbaum,et al.  Normal olfactory discrimination learning set and facilitation of reversal learning after medial-temporal damage in rats: implications for an account of preserved learning abilities in amnesia , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  E. Rolls,et al.  Visual responses of neurons in the dorsolateral amygdala of the alert monkey , 1979, Experimental Neurology.

[11]  Edmund T. Rolls,et al.  A theory of emotion and consciousness, and its application to understanding the neural basis of emotion. , 1995 .

[12]  Edmund T. Rolls,et al.  The responsiveness of neurons in the insular gustatory cortex of the macaque monkey is independent of hunger , 1988, Physiology & Behavior.

[13]  E. Rolls,et al.  Allocentric and egocentric spatial information processing in the hippocampal formation of the behaving primate , 1991, Psychobiology.

[14]  C. Geula,et al.  Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey , 1992, The Journal of comparative neurology.

[15]  M. Mishkin,et al.  Non-spatial memory after selective prefrontal lesions in monkeys , 1978, Brain Research.

[16]  E T Rolls,et al.  Information processing in the taste system of primates. , 1989, The Journal of experimental biology.

[17]  G. C. Baylis,et al.  Afferent connections of the caudolateral orbitofrontal cortex taste area of the primate , 1995, Neuroscience.

[18]  T. Tanabe,et al.  Discrimination of odors in olfactory bulb, pyriform-amygdaloid areas, and orbitofrontal cortex of the monkey. , 1975, Journal of neurophysiology.

[19]  E T Rolls,et al.  Olfactory neuronal responses in the primate orbitofrontal cortex: analysis in an olfactory discrimination task. , 1996, Journal of neurophysiology.

[20]  B. Slotnick,et al.  Olfactory Learning-Set Formation in Rats , 1974, Science.

[21]  Alan C. Evans,et al.  Functional localization and lateralization of human olfactory cortex , 1992, Nature.

[22]  D. R. Snyder,et al.  Alterations in aversive and aggressive behaviors following orbital frontal lesions in rhesus monkeys. , 1972, Acta neurobiologiae experimentalis.

[23]  E T Rolls,et al.  Gustatory responses of single neurons in the insula of the macaque monkey. , 1990, Journal of neurophysiology.

[24]  Edmund Rolls,et al.  Neural processing related to feeding in primates. , 1994 .

[25]  D. Pandya,et al.  Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey , 1989, The Journal of comparative neurology.

[26]  S. Takagi Olfactory Frontal Cortex and Multiple Olfactory Processing in Primates , 1991 .

[27]  E. T. Rolls,et al.  Hypothalamic neuronal responses associated with the sight of food , 1976, Brain Research.

[28]  Richard G. M. Morris,et al.  The enigma of olfactory learning , 1993, Trends in Neurosciences.

[29]  Charles M. Butter,et al.  Perseveration in extinction and in discrimination reversal tasks following selective frontal ablations in Macaca mulatta , 1969 .

[30]  J A Nevin,et al.  Olfactory discrimination, reversal learning, and stimulus control in rats. , 1975, Journal of comparative and physiological psychology.

[31]  E. Rolls,et al.  Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  E. Rolls,et al.  Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage , 1996, Neuropsychologia.

[33]  E. Rolls,et al.  Gustatory responses of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. , 1990, Journal of neurophysiology.

[34]  E. Rolls A Theory of Emotion, and its Application to Understanding the Neural Basis of Emotion , 1990 .

[35]  R. Passingham,et al.  Syndrome produced by lesions of the amygdala in monkeys (Macaca mulatta). , 1981, Journal of comparative and physiological psychology.

[36]  E. Rolls,et al.  The neural basis of brain-stimulation reward. , 1975, Progress in neurobiology.

[37]  E. Rolls The neural control of feeding in primates , 1993 .

[38]  E. Rolls The brain and reward , 1975 .

[39]  H. Barbas,et al.  Organization of cortical afferent input to orbitofrontal areas in the rhesus monkey , 1993, Neuroscience.

[40]  Edmund T. Rolls,et al.  Brain mechanisms for invariant visual and learning recognition , 1994 .

[41]  Joel L. Davis,et al.  Olfaction: A Model System for Computational Neuroscience , 1991 .

[42]  Edmund T. Rolls,et al.  Neurophysiology and functions of the primate amygdala. , 1992 .

[43]  H. Barbas Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey , 1988, The Journal of comparative neurology.

[44]  Edmund T. Rolls,et al.  The relative advantages of sparse versus distributed encoding for associative neuronal networks in the brain , 1990 .