- Email: [email protected]
Neuroscience: A More Dynamic View of the Social Brain
Current Biology Vol 22 No 23 R994
4. Nudds, R.L., and Dyke, G.J. (2010). Narrow primary feather rachises in Confuciusornis and Archaeopteryx suggest poor flight ability. Science 328, 887–889. 5. Longrich, N.R. (2006). Structure and function of hindlimb feathers in Archaeopteryx lithographica. Paleobiology 32, 417–431. 6. Xu, X., Zhou, Z.-H., Wang, X.-L., Kuang, X.-W., Zhang, F.-C., and Du, X.-K. (2003). Four-winged dinosaurs from China. Nature 421, 335–340. 7. Hu, D.Y., Hou, L.-H., Zhang, L.J., and Xu, X. (2009). A pre-Archaeopteryx troodontid from China with long feathers on the metatarsus. Nature 461, 640–643. 8. Longrich, N.R., Vinther, J., Meng, Q.J., Li, Q., and Russell, A.P. (2012). Primitive wing feather arrangement in Archaeopteryx lithographica and Anchiornis huxleyi. Curr. Biol. 22, 2262–2267. 9. Lucas, A.M., and Stettenheim, P.R. (1972). Avian anatomy: integument (Washington. D.C.: United States Department of Agriculture). 10. Rietschel, S. (1985). Feathers and wings of Archaeopteryx, and the question of her flight ability. In The beginnings of birds, M.K. Hecht, J.H. Ostrom, G. Viohl, and P. Wellnhofer, eds.
11.
12.
13.
14.
15.
16.
17.
(Eichstatt: Freunde des Jura-Museums), pp. 251–260. Hoyle, F., Wickramasinghe, N.C., and Rabilizirov, R. (1985). Archaeopteryx: Problems arise – and a motive. British Journal of Photography 132, 693–695. Feduccia, A., and Tordoff, H.B. (1979). Feathers of Archaeopteryx: asymmetric vanes indicate aerodynamic function. Science 203, 1021–1022. Senter, P. (2006). Scapular orientation in theropods and basal birds and the origin of flapping flight. Acta Palaeontol. Polonica 51, 305–313. Xu, X., You, H., Du, K., and Han, F. (2011). An Archaeopteryx-like theropod from China and the origin of Avialae. Nature 475, 465–470. Tucker, V.A. (1993). Gliding birds: reduction of induced drag by wing tip slots between the primary feathers. Journal of Experimental Biology 180, 285–310. Xu, X., and Guo, Y. (2009). The origin and early evolution of feathers: insights from recent paleontological and neontological data. Vertebrata Pal Asiatica 47, 311–329. Prum, R.O., and Brush, A.H. (2002). The evolutionary origin and diversification of
Neuroscience: A More Dynamic View of the Social Brain Information relevant for social interactions is thought to be processed in specific neural circuits. Recent studies shed new light on how that social information is encoded and processed by different brain areas. J. Sallet1, R.B. Mars1,2, and M.F.S. Rushworth1,2 Human and non-human primates are social animals and living in complex social environments has an impact on brain structure and function [1–3]. Social information is thought to be processed by a specific set of neural circuits often referred to as the ‘social brain’ [4–6]. How social information is encoded and the nature of the computations performed by different brain areas is nevertheless still debated. Papers in this issue of Current Biology by Watson and Platt [7] and Santiesteban et al. [8], focusing on the orbitofrontal cortex (OFC) and the temporo-parietal junction (TPJ), respectively (Figure 1), begin to unpick some of these issues. These two studies nicely complement recent observations on the roles of the OFC and TPJ from other laboratories [9,10]. Altogether, the results suggest that the context in which a social decision is taken strongly affects how the information is processed, suggesting a quite dynamic view of how social information is encoded and used by the social brain.
In their study, Watson and Platt [7] presented macaque monkeys with a simple decision-making task in which they could sacrifice juice to watch social images — pictures of other animals of various social statuses or pictures of female macaque perinea that male macaques appear to find intrinsically interesting. They found that neural activity in the OFC is modulated by both social and reward information, but most of the OFC neurons that show such modulated activity are either sensitive to reward or to social information [7]. This is one of the first tests of OFC single neuron activity in the social domain, but the result is broadly in line with previous reports that only a small proportion of OFC neurons multiplex values across reward dimensions [11]. It is interesting to compare the results of the Watson and Platt study [7] with those from the one other recent investigation of single neuron activity in OFC during social cognition. Azzi et al. [9] taught monkeys a simple oculomotor task in which their choices could lead to rewards either for just themselves or for a second animal too. The authors argue that the receipt of
feathers. Quarterly Review of Biology 77, 261–295. 18. Xu, X., Zheng, X.T., and You, H.L. (2010). Exceptional dinosaur fossils show ontogenetic development of early feathers. Nature 464, 1338–1341. 19. Lee, M.S.Y., and Worthy, T.H. (2011). Likelihood reinstates Archaeopteryx as a primitive bird. Biology letters. 20. Agnolı´n, F.L., and Novas, F.E. (2011). Unenlagiid theropods: are they members of the Dromaeosauridae (Theropoda, Maniraptora)? Anais Da Academia Brasileira de Ciencias 83, 117–162.
Institute of Vertebrate Paleontology and Paleonanthropology, Key Laboratory of Evolutionary Systematics of Vertebrates, Chinese Academy of Sciences, 142 Xiwai Street, Beijing, 100044, China. E-mail: [email protected]
http://dx.doi.org/10.1016/j.cub.2012.10.015
a reward by the second macaque apparently diminishes the value of rewards received by the first macaque. They found that lateral OFC neurons also reflect this apparent diminution of the reward value for the experimental animal when rewards are simultaneously given to another macaque. In other words, Azzi et al. [9] report the consequences of integrating both social and reward information in the firing rates of individual OFC neurons. These two studies, by Watson and Platt [7] and by Azzi et al. [9], can be seen to be complementary if one remembers that, in order to be able to learn the links that exist between choices and their outcomes, it is crucial to compute not only the scalar values of choice outcomes but also the identities of choice outcomes [12,13]. In other words, it is not just important whether an outcome is rewarding, but it is important to know what type of reward it is. One of the other key results reported by Watson and Platt [7] is the observation of a strong modulation of OFC activity by social categories (images with a dominant animal, a subordinate animal or with sexual content) — just what would be needed if the monkey is to learn about the precise category of outcome that is to be expected from a choice. But while it is essential to understand the identity of the outcome that is expected from a choice, it is also important to be able to compare the values of different outcomes on a single
Dispatch R995
papers. Such dynamism is not likely to be restricted to the ways in which a single brain area works but it is likely to be a feature of how areas interact in different configurations in order to mediate social cognition. References
Figure 1. Localization of the temporo-parietal junction on a human brain (left) and the orbitofrontal cortex on a macaque brain (right). The two brains are not represented at the same scale. Note that the localization in the macaque of an analogous area of the human TPJ is still debated. STS: superior temporal sulcus.
scale so that the preferred outcome can be ascertained. Both macaque and human studies are beginning to suggest that this second process might be more closely linked to medial OFC and adjacent ventromedial prefrontal cortex rather than lateral OFC [14–16]. Some evidence that such a process operates even in the social domain can be gleaned from the recent OFC recording studies, from the observation of a weak modulation of OFC activity by the value of social stimuli by Watson and Platt [7] and from the effect of the social status of the second macaque in the study by Azzi et al. [9]. One of the most dramatic ways in which the social context can affect cognition is when a person actually takes on the perspective of another person at the expense of their own perspective. The second study in Current Biology, by Santiesteban et al. [8], suggests that the TPJ is critical for such a change in social perspective. The authors applied transcranial direct current stimulation (tDCS), with the anode placed over the TPJ, while people performed various behavioral tasks in which either their own ‘self perspective’ or another’s perspective had to be considered. Such an electrode arrangement is thought likely to facilitate the operation of the TPJ. In
one task, the subjects were instructed to imitate a finger movement they saw on a screen or to make a different finger movement. In a second task, they were asked to suppress their own perspective on a scene and to adopt that of another person. In both cases, tDCS over TPJ was seen to induce improvements in performance. The findings reported by Santiesteban et al. [8] complement another recent study [10] in which subjects were asked to choose between two gambles to reward either themselves or someone else. The results of this experiment show that TPJ signals (as well as dorsomedial frontal signals) can flip between encoding the value to one’s own self of the choices that are being taken, or the value of a choice for another person [10]. The on-line control over which representation to use might depend on a learning mechanism that reports deviation from expectations. Such a mechanism has been associated with the TPJ [17]. A common theme of dynamic change — both of how outcome values are represented when alone and in a social context [7] and of how perspectives can be shifted between the personal and the social [8] — runs through the two new Current Biology
1. Sallet, J., Mars, R.B., Noonan, M.P., Andersson, J.L., O’Reilly, J.X., Jbabdi, S., Croxson, P.L., Jenkinson, M., Miller, K.L., and Rushworth, M.F. (2011). Social network size affects neural circuits in macaques. Science 334, 697–700. 2. Bickart, K.C., Wright, C.I., Dautoff, R.J., Dickerson, B.C., and Barrett, L.F. (2011). Amygdala volume and social network size in humans. Nat. Neurosci. 14, 163–164. 3. Dunbar, R.I., and Shultz, S. (2007). Evolution in the social brain. Science 317, 1344–1347. 4. Adolphs, R. (2009). The social brain: neural basis of social knowledge. Annu. Rev. Psychol. 60, 693–716. 5. Frith, C.D. (2007). The social brain? Philos. Trans. R. Soc. Lond. B. Biol. Sci. 362, 671–678. 6. Behrens, T.E., Hunt, L.T., and Rushworth, M.F. (2009). The computation of social behavior. Science 324, 1160–1164. 7. Watson, K.K., and Platt, M.L. (2012). Social signals in primate orbitofrontal cortex. Curr. Biol. 22, 2268–2273. 8. Santiesteban, I., Banissy, M.J., Catmur, C., and Bird, G. (2012). Enhancing social ability by stimulating the right temporoparietal junction. Curr. Biol. 22, 2274–2277. 9. Azzi, J.C., Sirigu, A., and Duhamel, J.R. (2012). Modulation of value representation by social context in the primate orbitofrontal cortex. Proc. Natl. Acad. Sci. USA 109, 4020. 10. Nicolle, A., Klein-Flu¨gge, M.C., Hunt, L.T., Vlaev, I., Dolan, R.J., and Behrens, T.E.J. (2012). An independent axis for executed and modeled choice in medial prefrontal cortex. Neuron 75, 1114–1121. 11. Kennerley, S.W., Behrens, T.E., and Wallis, J.D. (2011). Double dissociation of value computations in orbitofrontal and anterior cingulate neurons. Nat. Neurosci. 14, 1581–1589. 12. Niv, Y., and Schoenbaum, G. (2008). Dialogues on prediction errors. Trends Cogn. Sci. 12, 265–272. 13. Noonan, M.P., Mars, R.B., and Rushworth, M.F. (2011). Distinct roles of three frontal cortical areas in reward-guided behavior. J. Neurosci. 31, 14399–14412. 14. Noonan, M.P., Walton, M.E., Behrens, T.E., Sallet, J., Buckley, M.J., and Rushworth, M.F. (2010). Separate value comparison and learning mechanisms in macaque medial and lateral orbitofrontal cortex. Proc. Natl. Acad. Sci. USA 107, 20547–20552. 15. Rudebeck, P.H., and Murray, E.A. (2011). Balkanizing the primate orbitofrontal cortex: distinct subregions for comparing and contrasting values. Ann. N. Y. Acad. Sci. 1239, 1–13. 16. Bouret, S., and Richmond, B.J. (2010). Ventromedial and orbital prefrontalneurons differentially encode internally and externally driven motivational values in monkeys. J. Neurosci. 30, 8591–8601. 17. Suzuki, S., Harasawa, N., Ueno, K., Gardner, J.L., Ichinohe, N., Haruno, M., Cheng, K., and Nakahara, H. (2012). Learning to simulate other’s decisions. Neuron 74, 1125–1137. 1Department of Experimental Psychology, University of Oxford, Oxford, OX1 3UD, UK. 2Oxford Centre for Functional Magnetic Resonance Imaging of the Brain (FMRIB), University of Oxford, Oxford, OX1 3UD, UK. E-mail: [email protected]
http://dx.doi.org/10.1016/j.cub.2012.10.051
4. Nudds, R.L., and Dyke, G.J. (2010). Narrow primary feather rachises in Confuciusornis and Archaeopteryx suggest poor flight ability. Science 328, 887–889. 5. Longrich, N.R. (2006). Structure and function of hindlimb feathers in Archaeopteryx lithographica. Paleobiology 32, 417–431. 6. Xu, X., Zhou, Z.-H., Wang, X.-L., Kuang, X.-W., Zhang, F.-C., and Du, X.-K. (2003). Four-winged dinosaurs from China. Nature 421, 335–340. 7. Hu, D.Y., Hou, L.-H., Zhang, L.J., and Xu, X. (2009). A pre-Archaeopteryx troodontid from China with long feathers on the metatarsus. Nature 461, 640–643. 8. Longrich, N.R., Vinther, J., Meng, Q.J., Li, Q., and Russell, A.P. (2012). Primitive wing feather arrangement in Archaeopteryx lithographica and Anchiornis huxleyi. Curr. Biol. 22, 2262–2267. 9. Lucas, A.M., and Stettenheim, P.R. (1972). Avian anatomy: integument (Washington. D.C.: United States Department of Agriculture). 10. Rietschel, S. (1985). Feathers and wings of Archaeopteryx, and the question of her flight ability. In The beginnings of birds, M.K. Hecht, J.H. Ostrom, G. Viohl, and P. Wellnhofer, eds.
11.
12.
13.
14.
15.
16.
17.
(Eichstatt: Freunde des Jura-Museums), pp. 251–260. Hoyle, F., Wickramasinghe, N.C., and Rabilizirov, R. (1985). Archaeopteryx: Problems arise – and a motive. British Journal of Photography 132, 693–695. Feduccia, A., and Tordoff, H.B. (1979). Feathers of Archaeopteryx: asymmetric vanes indicate aerodynamic function. Science 203, 1021–1022. Senter, P. (2006). Scapular orientation in theropods and basal birds and the origin of flapping flight. Acta Palaeontol. Polonica 51, 305–313. Xu, X., You, H., Du, K., and Han, F. (2011). An Archaeopteryx-like theropod from China and the origin of Avialae. Nature 475, 465–470. Tucker, V.A. (1993). Gliding birds: reduction of induced drag by wing tip slots between the primary feathers. Journal of Experimental Biology 180, 285–310. Xu, X., and Guo, Y. (2009). The origin and early evolution of feathers: insights from recent paleontological and neontological data. Vertebrata Pal Asiatica 47, 311–329. Prum, R.O., and Brush, A.H. (2002). The evolutionary origin and diversification of
Neuroscience: A More Dynamic View of the Social Brain Information relevant for social interactions is thought to be processed in specific neural circuits. Recent studies shed new light on how that social information is encoded and processed by different brain areas. J. Sallet1, R.B. Mars1,2, and M.F.S. Rushworth1,2 Human and non-human primates are social animals and living in complex social environments has an impact on brain structure and function [1–3]. Social information is thought to be processed by a specific set of neural circuits often referred to as the ‘social brain’ [4–6]. How social information is encoded and the nature of the computations performed by different brain areas is nevertheless still debated. Papers in this issue of Current Biology by Watson and Platt [7] and Santiesteban et al. [8], focusing on the orbitofrontal cortex (OFC) and the temporo-parietal junction (TPJ), respectively (Figure 1), begin to unpick some of these issues. These two studies nicely complement recent observations on the roles of the OFC and TPJ from other laboratories [9,10]. Altogether, the results suggest that the context in which a social decision is taken strongly affects how the information is processed, suggesting a quite dynamic view of how social information is encoded and used by the social brain.
In their study, Watson and Platt [7] presented macaque monkeys with a simple decision-making task in which they could sacrifice juice to watch social images — pictures of other animals of various social statuses or pictures of female macaque perinea that male macaques appear to find intrinsically interesting. They found that neural activity in the OFC is modulated by both social and reward information, but most of the OFC neurons that show such modulated activity are either sensitive to reward or to social information [7]. This is one of the first tests of OFC single neuron activity in the social domain, but the result is broadly in line with previous reports that only a small proportion of OFC neurons multiplex values across reward dimensions [11]. It is interesting to compare the results of the Watson and Platt study [7] with those from the one other recent investigation of single neuron activity in OFC during social cognition. Azzi et al. [9] taught monkeys a simple oculomotor task in which their choices could lead to rewards either for just themselves or for a second animal too. The authors argue that the receipt of
feathers. Quarterly Review of Biology 77, 261–295. 18. Xu, X., Zheng, X.T., and You, H.L. (2010). Exceptional dinosaur fossils show ontogenetic development of early feathers. Nature 464, 1338–1341. 19. Lee, M.S.Y., and Worthy, T.H. (2011). Likelihood reinstates Archaeopteryx as a primitive bird. Biology letters. 20. Agnolı´n, F.L., and Novas, F.E. (2011). Unenlagiid theropods: are they members of the Dromaeosauridae (Theropoda, Maniraptora)? Anais Da Academia Brasileira de Ciencias 83, 117–162.
Institute of Vertebrate Paleontology and Paleonanthropology, Key Laboratory of Evolutionary Systematics of Vertebrates, Chinese Academy of Sciences, 142 Xiwai Street, Beijing, 100044, China. E-mail: [email protected]
http://dx.doi.org/10.1016/j.cub.2012.10.015
a reward by the second macaque apparently diminishes the value of rewards received by the first macaque. They found that lateral OFC neurons also reflect this apparent diminution of the reward value for the experimental animal when rewards are simultaneously given to another macaque. In other words, Azzi et al. [9] report the consequences of integrating both social and reward information in the firing rates of individual OFC neurons. These two studies, by Watson and Platt [7] and by Azzi et al. [9], can be seen to be complementary if one remembers that, in order to be able to learn the links that exist between choices and their outcomes, it is crucial to compute not only the scalar values of choice outcomes but also the identities of choice outcomes [12,13]. In other words, it is not just important whether an outcome is rewarding, but it is important to know what type of reward it is. One of the other key results reported by Watson and Platt [7] is the observation of a strong modulation of OFC activity by social categories (images with a dominant animal, a subordinate animal or with sexual content) — just what would be needed if the monkey is to learn about the precise category of outcome that is to be expected from a choice. But while it is essential to understand the identity of the outcome that is expected from a choice, it is also important to be able to compare the values of different outcomes on a single
Dispatch R995
papers. Such dynamism is not likely to be restricted to the ways in which a single brain area works but it is likely to be a feature of how areas interact in different configurations in order to mediate social cognition. References
Figure 1. Localization of the temporo-parietal junction on a human brain (left) and the orbitofrontal cortex on a macaque brain (right). The two brains are not represented at the same scale. Note that the localization in the macaque of an analogous area of the human TPJ is still debated. STS: superior temporal sulcus.
scale so that the preferred outcome can be ascertained. Both macaque and human studies are beginning to suggest that this second process might be more closely linked to medial OFC and adjacent ventromedial prefrontal cortex rather than lateral OFC [14–16]. Some evidence that such a process operates even in the social domain can be gleaned from the recent OFC recording studies, from the observation of a weak modulation of OFC activity by the value of social stimuli by Watson and Platt [7] and from the effect of the social status of the second macaque in the study by Azzi et al. [9]. One of the most dramatic ways in which the social context can affect cognition is when a person actually takes on the perspective of another person at the expense of their own perspective. The second study in Current Biology, by Santiesteban et al. [8], suggests that the TPJ is critical for such a change in social perspective. The authors applied transcranial direct current stimulation (tDCS), with the anode placed over the TPJ, while people performed various behavioral tasks in which either their own ‘self perspective’ or another’s perspective had to be considered. Such an electrode arrangement is thought likely to facilitate the operation of the TPJ. In
one task, the subjects were instructed to imitate a finger movement they saw on a screen or to make a different finger movement. In a second task, they were asked to suppress their own perspective on a scene and to adopt that of another person. In both cases, tDCS over TPJ was seen to induce improvements in performance. The findings reported by Santiesteban et al. [8] complement another recent study [10] in which subjects were asked to choose between two gambles to reward either themselves or someone else. The results of this experiment show that TPJ signals (as well as dorsomedial frontal signals) can flip between encoding the value to one’s own self of the choices that are being taken, or the value of a choice for another person [10]. The on-line control over which representation to use might depend on a learning mechanism that reports deviation from expectations. Such a mechanism has been associated with the TPJ [17]. A common theme of dynamic change — both of how outcome values are represented when alone and in a social context [7] and of how perspectives can be shifted between the personal and the social [8] — runs through the two new Current Biology
1. Sallet, J., Mars, R.B., Noonan, M.P., Andersson, J.L., O’Reilly, J.X., Jbabdi, S., Croxson, P.L., Jenkinson, M., Miller, K.L., and Rushworth, M.F. (2011). Social network size affects neural circuits in macaques. Science 334, 697–700. 2. Bickart, K.C., Wright, C.I., Dautoff, R.J., Dickerson, B.C., and Barrett, L.F. (2011). Amygdala volume and social network size in humans. Nat. Neurosci. 14, 163–164. 3. Dunbar, R.I., and Shultz, S. (2007). Evolution in the social brain. Science 317, 1344–1347. 4. Adolphs, R. (2009). The social brain: neural basis of social knowledge. Annu. Rev. Psychol. 60, 693–716. 5. Frith, C.D. (2007). The social brain? Philos. Trans. R. Soc. Lond. B. Biol. Sci. 362, 671–678. 6. Behrens, T.E., Hunt, L.T., and Rushworth, M.F. (2009). The computation of social behavior. Science 324, 1160–1164. 7. Watson, K.K., and Platt, M.L. (2012). Social signals in primate orbitofrontal cortex. Curr. Biol. 22, 2268–2273. 8. Santiesteban, I., Banissy, M.J., Catmur, C., and Bird, G. (2012). Enhancing social ability by stimulating the right temporoparietal junction. Curr. Biol. 22, 2274–2277. 9. Azzi, J.C., Sirigu, A., and Duhamel, J.R. (2012). Modulation of value representation by social context in the primate orbitofrontal cortex. Proc. Natl. Acad. Sci. USA 109, 4020. 10. Nicolle, A., Klein-Flu¨gge, M.C., Hunt, L.T., Vlaev, I., Dolan, R.J., and Behrens, T.E.J. (2012). An independent axis for executed and modeled choice in medial prefrontal cortex. Neuron 75, 1114–1121. 11. Kennerley, S.W., Behrens, T.E., and Wallis, J.D. (2011). Double dissociation of value computations in orbitofrontal and anterior cingulate neurons. Nat. Neurosci. 14, 1581–1589. 12. Niv, Y., and Schoenbaum, G. (2008). Dialogues on prediction errors. Trends Cogn. Sci. 12, 265–272. 13. Noonan, M.P., Mars, R.B., and Rushworth, M.F. (2011). Distinct roles of three frontal cortical areas in reward-guided behavior. J. Neurosci. 31, 14399–14412. 14. Noonan, M.P., Walton, M.E., Behrens, T.E., Sallet, J., Buckley, M.J., and Rushworth, M.F. (2010). Separate value comparison and learning mechanisms in macaque medial and lateral orbitofrontal cortex. Proc. Natl. Acad. Sci. USA 107, 20547–20552. 15. Rudebeck, P.H., and Murray, E.A. (2011). Balkanizing the primate orbitofrontal cortex: distinct subregions for comparing and contrasting values. Ann. N. Y. Acad. Sci. 1239, 1–13. 16. Bouret, S., and Richmond, B.J. (2010). Ventromedial and orbital prefrontalneurons differentially encode internally and externally driven motivational values in monkeys. J. Neurosci. 30, 8591–8601. 17. Suzuki, S., Harasawa, N., Ueno, K., Gardner, J.L., Ichinohe, N., Haruno, M., Cheng, K., and Nakahara, H. (2012). Learning to simulate other’s decisions. Neuron 74, 1125–1137. 1Department of Experimental Psychology, University of Oxford, Oxford, OX1 3UD, UK. 2Oxford Centre for Functional Magnetic Resonance Imaging of the Brain (FMRIB), University of Oxford, Oxford, OX1 3UD, UK. E-mail: [email protected]
http://dx.doi.org/10.1016/j.cub.2012.10.051