Abstract
Neurons with responses selective for faces are described in the macaque orbitofrontal cortex. The neurons typically respond 2–13 times more to the best face than to the best non-face stimulus, and have response latencies which are typically in the range of 130–220 ms. Some of these face-selective neurons respond to identity, and others to facial expression. Some of the neurons do not have different responses to different views of a face, which is a useful property of neurons responding to face identity. Other neurons have view-dependent responses, and some respond to moving but not still heads. The neurons with face expression, face movement, or face view-dependent responses would all be useful as part of a system decoding and representing signals important in social interactions. The representation of face identity is also important in social interactions, for it provides some of the information needed in order to make different responses to different individuals. In addition, some orbitofrontal cortex neurons were shown to be tuned to auditory stimuli, including for some neurons, the sound of vocalizations. The findings are relevant to understanding the functions of the primate including human orbitofrontal cortex in normal behaviour, and to understanding the effects of damage to this region in humans.
Similar content being viewed by others
References
Aggleton JP, Passingham RE (1981) Stereotaxic surgery under X-ray guidance in the rhesus monkey, with special reference to the amygdala. Exp Brain Res 44:271–276
Barbas H (1988) Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey. J Comp Neurol 276:313–342
Barbas H (1993) Organization of cortical afferent input to the orbitofrontal area in the rhesus monkey. Neuroscience 56:841–864
Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex. Neurosci Biobehav Rev 19:499–510
Baxter MG, Parker A, Lindner CC, Izquierdo AD, Murray EA (2000) Control of response selection by reinforcer value requires interaction of amygdala and orbital prefrontal cortex. J Neurosci 20:4311–4319
Baylis GC, Rolls ET, Leonard CM (1985) Selectivity between faces in the responses of a population of neurons in the cortex in the superior temporal sulcus of the monkey. Brain Res 342:91–102
Baylis GC, Rolls ET, Leonard CM (1987) Functional subdivisions of the temporal lobe neocortex. J Neurosci 7:330–342
Baylis LL, Rolls ET, Baylis GC (1994) Afferent connections of the orbitofrontal cortex taste area of the primate. Neuroscience 64:801–812
Berlin H, Rolls ET, Kischka U (2004) Impulsivity, time perception, emotion, and reinforcement sensitivity in patients with orbitofrontal cortex lesions. Brain 127:1108–1126
Bruce C, Desimone R, Gross CG (1981) Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. J Neurophysiol 46:369–384
Butter CM (1969) Perseveration in extinction and in discrimination reversal tasks following selective prefrontal ablations in Macaca mulatta. Physiol Behav 4:163–171
Carmichael ST, Price JL (1994) Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. J Comp Neurol 346:366–402
Carmichael ST, Price JL (1996) Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol 371:179–207
Cavada C, Company T, Tejedor J, Cruz-Rizzolo RJ, Reinoso-Suarez F (2000) The anatomical connecitions of the macaque monkey orbitofrontal cortex:a review. Cereb Cortex 10:220–242
Critchley HD, Rolls ET (1996a) Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex. J Neurophysiol 75:1673–1686
Critchley HD, Rolls ET (1996b) Olfactory neuronal responses in the primate orbitofrontal cortex: analysis in an olfactory discrimination task. J Neurophysiol 75:1659–1672
Critchley HD, Rolls ET (1996c) Responses of primate taste cortex neurons to the astringent tastant tannic acid. Chem Senses 21:135–145
Deco G, Rolls ET (2005) Synaptic and spiking dynamics underlying reward reversal in orbitofrontal cortex. Cereb Cortex 15:15–30
Desimone R, Albright TD, Gross CG, Bruce C (1984) Stimulus-selective properties of inferior temporal neurons in the macaque. J Neurosci 4:2051–2062
Fellows LK, Farah MJ (2003) Ventromedial frontal cortex mediates affective shifting in humans: evidence from a reversal learning paradigm. Brain 126:1830–1837
Fisher RA (1932) Statistical methods for research workers. Oliver and Boyd, London
Franco L, Rolls ET, Aggelopoulos NC, Treves A (2004) The use of decoding to analyze the contribution to the information of the correlations between the firing of simultaneously recorded neurons. Exp Brain Res 155:370–384
Fuster JM (1997) The prefrontal cortex. Raven Press, New York
Hackett TA, Stepniewska I, Kaas JH (1999) Prefrontal connections of the parabelt auditory cortex in macaque monkeys. Brain Res 817:45–58
Hasselmo ME, Rolls ET, Baylis GC (1989a) The role of expression and identity in the face-selective responses of neurons in the temporal visual cortex of the monkey. Behav Brain Res 32:203–218
Hasselmo ME, Rolls ET, Baylis GC, Nalwa V (1989b) Object-centred encoding by face-selective neurons in the cortex in the superior temporal sulcus of the the monkey. Exp Brain Res 75:417–429
Hornak J, Rolls ET, Wade D (1996) Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage. Neuropsychologia 34:247–261
Hornak J, Bramham J, Rolls ET, Morris RG, O’Doherty J, Bullock PR, Polkey CE (2003) Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices. Brain 126:1691–1712
Hornak J, O’Doherty J, Bramham J, Rolls ET, Morris RG, Bullock PR, Polkey CE (2004) Reward-related reversal learning after surgical excisions in orbitofrontal and dorsolateral prefrontal cortex in humans. J Cogn Neurosci 16:463–478
Izquierdo A, Suda RK, Murray EA (2004) Bilateral orbital prefrontal cortex lesions in rhesus monkeys disrupt choices guided by both reward value and reward contingency. J Neurosci 24:7540–7548
Jolly A (1972) The evolution of primate behaviour. Macmillan, New York
Jurgens U (2002) Neural pathways underlying vocal control. Neurosci Biobehav Rev 26:235–258
Kirk RE (1995) Experimental design: procedures for the behavioural sciences. Brooks/Cole, Pacific Grove
Kringelbach ML, Rolls ET (2004) The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Progress Neurobiol 72:341–372
Kringelbach ML, Rolls ET, de Araujo IET (2003) Neural correlates of rapid reversal learning in a simple model of human social interaction. NeuroImage 20:1371–1383
Leonard CM, Rolls ET, Wilson FAW, Baylis GC (1985) Neurons in the amygdala of the monkey with responses selective for faces. Behav Brain Res 15:159–176
Lipton PA, Alvarez P, Eichenbaum H (1999) Crossmodal associative memory representations in rodent orbitofrontal cortex. Neuron 22:349–359
Littell RC, Folks JL (1971) Asymptotic optimality of Fisher’s method of combining independent tests. J Am Stat Assoc 66:802–806
O’Doherty J, Winston J, Critchley H, Perrett D, Burt DM, Dolan RJ (2003) Beauty in a smile: the role of medical orbitofrontal cortex in facial attractiveness. Neuropsychologia 41:147–155
O’Scalaidhe SP, Wilson FA, Goldman-Rakic PS (1997) Areal segregation of face-processing neurons in prefrontal cortex. Science 278:1135–1138
Pandya DN, Kuypers HGJM (1969) Cortico-cortical connections in the rhesus monkey. Brain Res 13:13–36
Pears A, Parkinson JA, Hopewell L, Everitt BJ, Roberts AC (2003) Lesions of the orbitofrontal but not medial prefrontal cortex disrupt conditioned reinforcement in primates. J Neurosci 23:11189–11201
Perrett DI, Rolls ET, Caan W (1982) Visual neurons responsive to faces in the monkey temporal cortex. Exp Brain Res 47:329–342
Pigarev IN, Rizzolatti G, Scandolara C (1979) Neurons responding to visual stimuli in the frontal lobe of macaque monkeys. Neurosci Lett 12:207–212
Poremba A, Saunders RC, Crane AM, Cook M, Sokoloff L, Mishkin M (2003) Functional mapping of the primate auditory system. Science 299:568–572
Rolls ET (1990) A theory of emotion, and its application to understanding the neural basis of emotion. Cogn Emotion 4:161–190
Rolls ET (1992) Neurophysiological mechanisms underlying face processing within and beyond the temporal cortical visual areas. Philos Trans R Soc Lond B 335:11–21
Rolls ET (1996) The orbitofrontal cortex. Philos Trans R Soc Lond B 351:1433–1444
Rolls ET (1999a) The brain and emotion. Oxford University Press, Oxford
Rolls ET (1999b) The functions of the orbitofrontal cortex. Neurocase 5:301–312
Rolls ET (2000a) Functions of the primate temporal lobe cortical visual areas in invariant visual object and face recognition. Neuron 27:205–218
Rolls ET (2000b) The orbitofrontal cortex and reward. Cereb Cortex 10:284–294
Rolls ET (2002) The functions of the orbitofrontal cortex. In: Stuss DT, Knight RT (ed) Principles of frontal lobe function. Oxford University Press, New York, Chap 23, pp 354–375
Rolls ET (2005) Emotion explained. Oxford University Press, Oxford
Rolls ET, Baylis LL (1994) Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex. J Neurosci 14:5437–5452
Rolls ET, Deco G (2002) Computational neuroscience of vision. Oxford University Press, Oxford
Rolls ET, Tovee MJ (1995) Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. J Neurophysiol 73:713–726
Rolls ET, Treves A (1998) Neural networks and brain function. Oxford University Press, Oxford
Rolls ET, Sienkiewicz ZJ, Yaxley S (1989) Hunger modulates the responses to gustatory stimuli of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. Eur J Neurosci 1:53–60
Rolls ET, Yaxley S, Sienkiewicz ZJ (1990) Gustatory responses of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. J Neurophysiol 64:1055–1066
Rolls ET, Hornak J, Wade D, McGrath J (1994) Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. J Neurol, Neurosurg Psychiatr 57:1518–1524
Rolls ET, Critchley H, Wakeman EA, Mason R (1996a) Responses of neurons in the primate taste cortex to the glutamate ion and to inosine 5′-monophosphate. Physiol Behav 59:991–1000
Rolls ET, Critchley HD, Mason R, Wakeman EA (1996b) Orbitofrontal cortex neurons: role in olfactory and visual association learning. J Neurophysiol 75:1970–1981
Rolls ET, Critchley HD, Treves A (1996c) The representation of olfactory information in the primate orbitofrontal cortex. J Neurophysiol 75:1982–1996
Rolls ET, Treves A, Tovee MJ (1997) The representational capacity of the distributed encoding of information provided by populations of neurons in the primate temporal visual cortex. Exp Brain Res 114:177–185
Rolls ET, Aggelopoulos NC, Franco L, Treves A (2004) Information encoding in the inferior temporal cortex: contributions of the firing rates and correlations between the firing of neurons. Biol Cybern 90:19–32
Rolls ET, Browning AS, Inoue K, Hernadi S (2005) Novel visual stimuli activate a population of neurons in the primate orbitofrontal cortex. Neurobiol Learn Mem 84(2):111–123
Romanski LM, Goldman-Rakic PS (2001) An auditory domain in primate prefrontal cortex. Nat Neurosci 5:15–16
Romanski LM, Tian B, Fritz J, Mishkin M, Goldman-Rakic PS, Rauschecker JP (1999) Dual streams of auditory afferents target multiple domains in the primate orbitofrontal cortex. Nat Neurosci 2:1131–1136
Schultz W, Tremblay L, Hollerman JR (2000) Reward processing in primate orbitofrontal cortex and basal ganglia. Cereb Cortex 10:272–284
Tanaka K (1996) Inferotemporal cortex and object vision. Annu Rev Neurosci 19:109–139
Thorpe SJ, Rolls ET, Maddison S (1983) Neuronal activity in the orbitofrontal cortex of the behaving monkey. Exp Brain Res 49:93–115
Tovee MJ, Rolls ET, Azzopardi P (1994) Translation invariance in the responses to faces of single neurons in the temporal visual cortical areas of the alert macaque. J Neurophysiol 72:1049–1060
Tremblay L, Schultz W (2000) Modifications of reward expectation-related neuronal activity during learning in primate orbitofrontal cortex. J Neurophysiol 83:1877–1885
Treves A, Panzeri S, Rolls ET, Booth M, Wakeman EA (1999) Firing rate distributions and efficiency of information transmission of inferior temporal cortex neurons to natural visual stimuli. Neural Comput 11:611–641
Van Dobben De Bruyn CS (1968) Cumulative sum tests: theory and practice. Griffin, London
Wallis G, Rolls ET (1997) Invariant face and object recognition in the visual system. Progress Neurobiol 51:167–194
Webster MJ, Bachevalier J, Ungerleider LG (1994) Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. Cereb Cortex 4:470–483
Wilson FAW, O’Scalaidhe SPO, Goldman-Rakic PS (1993) Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 260:1955–1958
Woodward RH, Goldsmith PL (1964) Cumulative sum techniques. Oliver & Boyd, Edinburgh
Zaykin DV, Zhivotovsky LA, Westfall PH, Weir BS (2002) Truncated product method for combining P-values. Genet Epidemiol 22:170–185
Acknowledgement
This research was supported by Medical Research Council Grant PG9826105.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rolls, E.T., Critchley, H.D., Browning, A.S. et al. Face-selective and auditory neurons in the primate orbitofrontal cortex. Exp Brain Res 170, 74–87 (2006). https://doi.org/10.1007/s00221-005-0191-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-005-0191-y