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The orbitofrontal cortex: Neuronal activity in the behaving monkey

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Summary

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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References

  • Benevento LA, Fallon JH, Davis BJ, Rezak M (1977) Auditory-visual interaction in single cells of the superior temporal sulcus and orbito-frontal cortex of the macaque monkey. Exp Neurol 57: 849–872

    Article  CAS  PubMed  Google Scholar 

  • Benjamin RM, Jackson JC (1974) Unit discharges in the mediodorsal nucleus of the squirrel monkey evoked by electrical stimulation of the olfactory bulb. Brain Res 75: 181–191

    Google Scholar 

  • Bos J, Benevento LA (1975) Projections of the medial pulvinar to orbitofrontal cortex and frontal eye fields in the rhesus monkey. Exp Neurol 49: 487–496

    Google Scholar 

  • Brutkowski S, Mishkin M, Rosvold HE (1963) Positive and inhibitory motor conditioned reflexes in monkeys after ablation of orbital or dorso-lateral surface of the frontal cortex. In: Gutman E, Hnik P (eds) Central and peripheral mechanisms of motor functions. Czechoslovak Academy of Sciences, Prague, pp 133–141

    Google Scholar 

  • Burton MJ, Rolls ET, Mora F (1976) Effects of hunger on the responses of neurons in the lateral hypothalamus to the sight and taste of food. Exp Neurol 51: 668–677

    Google Scholar 

  • Butter CM (1969) Perseveration in extinction and in discrimination reversal tasks following selective frontal ablations in Macaca mulatta. Physiol Behav 4: 163–171

    Google Scholar 

  • Butter CM, Mishkin M, Rosvold HE (1963) Conditioning and extinction of a food-rewarded response after selective ablations of frontal cortex in rhesus monkeys. Exp Neurol 7: 65–75

    Google Scholar 

  • Butter CM, Mishkin M, Mirsky AF (1968) Emotional responses toward humans in monkeys with selective frontal lesions. Physiol Behav 3: 213–215

    Google Scholar 

  • Butter CM, McDonald JA, Snyder DA (1969) Orality, preference behavior, and reinforcement value of nonfood objects in monkeys with orbital frontal lesions. Science 164: 1306–1307

    Google Scholar 

  • Butter CM, Snyder DR, McDonald JA (1970) Effects of orbitofrontal lesions on aversive and aggressive behaviours in rhesus monkeys. J Comp Physiol Psychol 72: 132–144

    Google Scholar 

  • Butter CM, Snyder DR (1972) Alterations in aversive and aggressive behaviors following orbitofrontal lesions in rhesus monkeys. Acta Neurobiol Exp (Warsz) 32: 525–565

    Google Scholar 

  • Chavis DA, Pandya DN (1976) Further observations on the corticofrontal connections in rhesus monkey. Brain Res 117: 369–386

    Google Scholar 

  • Fuster JM (1980) The Prefrontal cortex. Raven Press, New York

    Google Scholar 

  • Goldberg ME, Bushnell MC (1981) Behavioral enhancement of visual responses in monkey cerebral cortex. II. Modulation in frontal eye fields specifically related to saccades. J Neurophysiol 46: 773–787

    Google Scholar 

  • Iversen SD, Mishkin M (1970) Perseverative interference in monkey following selective lesions of the inferior prefrontal convexity. Exp Brain Res 11: 376–386

    CAS  PubMed  Google Scholar 

  • Jacobsen S, Butters N, Kowalski H (1978) Subcortical projections to the orbital region of the frontal lobe. Soc Neurosci Abstr 4: 222

    Google Scholar 

  • Jones B, Mishkin M (1972) Limbic lesions and the problem of stimulus-reinforcement associations. Exp Neurol 36: 362–377

    Article  CAS  PubMed  Google Scholar 

  • Jones EG (1969) Interrelationships of parieto-temporal and frontal cortex in the rhesus monkey. Brain Res 13: 412–415

    Google Scholar 

  • Jones EG, Powell TPS (1970) An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 93: 793–821

    CAS  PubMed  Google Scholar 

  • Kojima S (1980) Prefrontal unit activity in the monkey: Relation to visual stimuli and movements. Exp Neurol 69: 110–123

    Google Scholar 

  • Kubota K, Iwamoto T, Suzuki H (1974) Visuokinetic activities of primate prefrontal neurons during delayed-response performance. J Neurophysiol 37: 1197–1212

    Google Scholar 

  • Kuypers HGJM, Szwarcbart MK, Mishkin M, Rosvold HE (1965) Occipitotemporal corticocortical connections in the rhesus monkey. Exp Neurol 11: 245–262

    Google Scholar 

  • Lawicka W, Mishkin M, Rosvold HE (1966) Dissociation of impairment on auditory tasks following orbital and dorsolateral frontal lesions in monkeys. Proc X Congr Pol Physiol Soc, Warshaw, pp 178–179

  • Lawicka W, Mishkin M, Rosvold HE (1975) Dissociation of deficits on auditory tasks following partial prefrontal lesions in monkeys. Acta Neurobiol Exp (Warsz) 35: 584–607

    Google Scholar 

  • Markowitsch HJ, Pritzel M (1976) Reward-related neurons in cat association cortex. Brain Res 111: 185–188

    Google Scholar 

  • Markowitsch HJ, Pritzel M (1978) Single-unit activity in cat prefrontal and posterior parietal cortex during performance of spatial reversal tasks. Brain Res 149: 53–76

    Google Scholar 

  • Merrill EG, Ainsworth A (1972) Glass-coated platinum-plated tungsten microelectrodes. Med Biol Eng 10: 662–672

    Google Scholar 

  • Mikami A, Ito S, Kubota K (1978) Responses of prefrontal neurons to extrafoveal slit stimulation in a visual fixation task of monkeys. J Physiol Soc Japan 40: 269

    Google Scholar 

  • Milner B (1964) Some effects of frontal lobectomy in man. In: Warren JM, Akert K (eds) The frontal granular cortex and behavior. McGraw-Hill, New York, pp 313–334

    Google Scholar 

  • Mishkin M (1964) Perseveration of central sets after frontal lesions in monkeys. In: Warren JM, Akert K (eds) The frontal granular cortex and behavior. McGraw Hill, New York, pp 219–241

    Google Scholar 

  • Mishkin M, Manning FJ (1978) Non-spatial memory after selective prefrontal lesions in monkeys. Brain Res 143: 313–324

    Google Scholar 

  • Mishkin M, Vest B, Waxler M, Rosvold HE (1969) A reexamination of the effects of frontal lobe lesions on object alternation. Neuropsychologia 7: 357–363

    Google Scholar 

  • Mohler CW, Goldberg ME, Wurtz RH (1973) Visual receptive fields of frontal eye field neurons. Brain Res 61: 385–389

    Google Scholar 

  • Mora F, Avrith DB, Phillips AG, Rolls ET (1979) Effects of satiety on self-stimulation of the orbitofrontal cortex in the monkey. Neurosci Lett 13: 141–145

    Google Scholar 

  • Nauta WJH (1971) The problem of the frontal lobe: A reinterpretation. J Psychiatr Res 8: 167–187

    Google Scholar 

  • Nauta WJH (1972) Neural associations of the frontal cortex. Acta Neurobiol Exp (Warsz) 32: 125–140

    Google Scholar 

  • Niki H, Sakai M, Kubota K (1972) Delayed alternation performance and unit activity of the caudate head and medial orbitofrontal gyrus in the monkey. Brain Res 38: 343–353

    Google Scholar 

  • Niki H, Watanabe M (1979) Prefrontal and cingulate unit activity during timing behavior in the monkey. Brain Res 171: 213–224

    Google Scholar 

  • Pandya DN, Kuypers H (1969) Cortico-cortical connections in the rhesus monkey. Brain Res 13: 13–36

    Google Scholar 

  • Pigarev IN, Rizzolatti G, Scandolara C (1979) Neurons responding to visual stimuli in the frontal lobe of macaque monkeys. Neurosci Lett 12: 207–212

    Google Scholar 

  • Potter H, Nauta WJH (1979) A note on the problem of olfactory associations of the orbitofrontal cortex in the monkey. Neuroscience 4: 361–367

    Google Scholar 

  • Rizzolatti G, Scandolara C, Matelli M, Gentilluci M (1981) Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses. Behav Brain Res 2: 147–164

    Article  CAS  PubMed  Google Scholar 

  • Rolls ET (1975) The brain and reward. Pergamon Press, Oxford

    Google Scholar 

  • Rolls ET (1981) Processing beyond the inferior temporal visual cortex related to feeding, learning, and striatal function. In: Katsuki Y, Norgren R, Sato M (eds) Brain mechanisms of sensation, chapt 16. Wiley, New York, pp 241–269

    Google Scholar 

  • Rolls ET, Burton MJ, Mora F (1976) Hypothalamic neuronal responses associated with the sight of food. Brain Res 111: 53–66

    Google Scholar 

  • Rolls ET, Judge SJ, Sanghera MK (1977) Activity of neurons in the inferotemporal cortex of the alert monkey. Brain Res 130: 229–238

    Google Scholar 

  • Rolls ET, Sanghera MK, Roper-Hall A (1979) The latency of activation of neurons in the lateral hypothalamus and substantia innominata during feeding in the monkey. Brain Res 164: 121–135

    Google Scholar 

  • Rolls ET, Burton MJ, Mora F (1980) Neurophysiological analysis of brain-stimulation reward in the monkey. Brain Res 194: 339–357

    Google Scholar 

  • Rosenkilde CE, Bauer RH, Fuster JM (1981) Single-unit activity in ventral prefrontal cortex of behaving monkeys. Brain Res 209: 375–394

    Google Scholar 

  • Sanghera MK, Rolls ET, Roper-Hall A (1979) Visual responses of neurons in the dorsolateral amygdala of the alert monkey. Exp Neurol 63: 610–626

    Google Scholar 

  • Suzuki H, Azuma M (1977) Prefrontal unit activity during gazing at a light spot in the monkey. Brain Res 126: 497–508

    Google Scholar 

  • Suzuki H, Azuma M, Yumiya H (1979) Stimulus and behavioural factors contributing to the activation of monkey prefrontal neurons during gazing. Jpn J Physiol 29: 471–490

    Google Scholar 

  • Tanabe T, Yarita H, Iino M, Ooshima Y, Takagi SR (1975) An olfactory projection area in the orbitofrontal cortex of the monkey. J Neurophysiol 38: 1269–1283

    Google Scholar 

  • Tanaka D (1973) Effects of selective prefrontal decortication on escape behavior in the monkey. Brain Res 53: 161–173

    Google Scholar 

  • Thorpe SJ, Maddison S, Rolls ET (1979) Single unit activity in the orbitofrontal cortex of the behaving animal. Neurosci Lett 3: S77

    Google Scholar 

  • Ursin H, Rosvold HE, Vest B (1969) Food preference in brain lesioned monkeys. Physiol Behav 4: 609–612

    Google Scholar 

  • Watanabe M (1982) Prefrontal unit activity during delayed conditional discriminations in the monkey. Brain Res 225: 51–66

    Google Scholar 

  • Woodward RR, Goldsmith PL (1964) Cumulative sum techniques. Mathematical and statistical techniques for industry. ICI Monograph, no. 3. Oliver and Boyd, Edinburgh

    Google Scholar 

  • Wurtz RH, Mohler CW (1976) Enhancement of visual responses in monkey striate cortex and frontal eye fields. J Neurophysiol 39: 766–772

    Google Scholar 

  • Yarita H, Iino M, Tanabe T, Kogure S, Takagi SF (1980) A transthalamic olfactory pathway to orbitofrontal cortex in the monkey. J Neurophysiol 43: 69–85

    Google Scholar 

Download references

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Thorpe, S.J., Rolls, E.T. & Maddison, S. The orbitofrontal cortex: Neuronal activity in the behaving monkey. Exp Brain Res 49, 93–115 (1983). https://doi.org/10.1007/BF00235545

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