Neuron
Previews Laeng, B., Sirois, S., and Gredeba¨ck, G. (2012). Perspect. Psychol. Sci. 7, 18–27.
Polack, P.O., Friedman, J., and Golshani, P. (2013). Nat. Neurosci. 16, 1331–1339.
McGinley, M.J., David, S.V., and McCormick, D.A. (2015). Neuron 87, this issue, 179–192.
Posner, M.I., and Rothbart, M.K. (2000). Dev. Psychopathol. 12, 427–441.
Niell, C.M., and Stryker, M.P. (2010). Neuron 65, 472–479.
Poulet, J.F., and Petersen, C.C. (2008). Nature 454, 881–885.
Pinto, L., Goard, M.J., Estandian, D., Xu, M., Kwan, A.C., Lee, S.H., Harrison, T.C., Feng, G., and Dan, Y. (2013). Nat. Neurosci. 16, 1857–1863.
Reimer, J., Froudarakis, E., Cadwell, C.R., Yatsenko, D., Denfield, G.H., and Tolias, A.S. (2014). Neuron 84, 355–362.
Saleem, A.B., Ayaz, A., Jeffery, K.J., Harris, K.D., and Carandini, M. (2013). Nat. Neurosci. 16, 1864–1869. Schneider, D.M., Nelson, A., and Mooney, R. (2014). Nature 513, 189–194. Vinck, M., Batista-Brito, R., Knoblich, U., and Cardin, J.A. (2015). Neuron 86, 740–754. Yerkes, R.M., and Dodson, J. (1908). J. Comp. Neurol. Psychol. 18, 459–482.
The Hippocampus as a Cognitive Map . of Social Space Howard Eichenbaum1,* 1Center for Memory and Brain, Boston University, Boston, MA 02215, USA *Correspondence: [email protected] http://dx.doi.org/10.1016/j.neuron.2015.06.013
The traditional view of the hippocampus is that it creates a cognitive map to navigate physical space. Here, in this issue of Neuron, Tavares et al. (2015) show that the human hippocampus maps dimensions of social space, indicating a function in the service of navigating everyday life. Edward C. Tolman (Tolman, 1948) developed the notion of cognitive maps as a heuristic for understanding the complex cognitive mechanisms that guide behavior. His theory of purposeful behavior was aimed to contrast with the contemporaneous, widely accepted view that behavior is guided by stimulusresponse connections, and his experiments identified specific abilities that reflected cognition outside the scope of behavior that could be supported by stimulus-response learning. Tolman’s experiments focused on rats solving maze problems, but he did not interpret his findings narrowly as a description of navigational computations. Rather, he employed spatial learning to model aspects of goal-oriented decision-making, and he viewed a cognitive map as an organization of cognitive operations. Tolman emphasized that cognitive maps provide insights into human cognition broadly, including human social behavior. In this issue of Neuron, Tavares et al. (2015) realize Tolman’s broader view of cognitive maps by their characterization of a cognitive map of social organization in humans supported by the hippocampus.
A connection between the hippocampus and cognitive maps began with a landmark book by O’Keefe and Nadel (1978), who proposed that the hippocampus provided the neural basis of cognitive mapping. The book, and decades of experiments and theoretical work that followed, departed from Tolman’s map of cognition to instead focus on cognitive maps as psychological and neural representations of physical space, and on mechanisms within the hippocampus and associated brain areas that create geographical maps and perform navigational computations (Hartley et al., 2014). Originally, O’Keefe and Nadel (1978) extended their model to the representation of items and events in spatialtemporal context as an evolutionary advance of the human hippocampus to support its function in mapping memories, particularly as it might represent the deep structure of language. This extension of their theory clearly went beyond physical space (although only for humans) and, in doing so, acknowledged that information processing by the hippocampus can in principle be applied outside the domain of physical
space. To what non-spatial domains does it apply? Tavares et al. (2015) here reveal that cognitive maps in the hippocampus extend to social space. Social space is an excellent candidate for hippocampal representation, because it is a domain that, like physical space, is characterized by a combination of continuous dimensions. So, just as planar geography is characterized by two spatial dimensions, social space has been characterized by multiple social dimensions, including of particular relevance here, the dimensions of power and affiliation. Importantly, just as the dimensions of geographic space are defined in terms of continuous metrics of physical distance, power and affiliation are defined in terms of continuous metrics of social distance. To test the idea that social relations are mapped within the hippocampus, Tavares et al. (2015) designed a role-playing game in which participants imagined they had moved to a new town and their goal was to find a job and place to live. To accomplish this, the participants conversed with local people in the search for a job or home through different Neuron 87, July 1, 2015 ª2015 Elsevier Inc. 9
Neuron
Previews
responses in which they could hippocampal volume gray comply with a character’s dematter is increased during mand or make demands medical training, although (increasing or decreasing the Woollett et al., (2008) reported power of the character) and that medical doctors do not engage or not engage in perhave larger hippocampi, sonal conversation and physwhereas London taxi drivers ical interaction (increasing or do. Most intriguing is a report decreasing affiliation with the that professional piano tuners character), and the accumulawho spend thousands of hours tion of successive interacnavigating acoustic scenes tions took the narrative in have larger hippocampal gray different directions. The outmatter volumes associated comes of these social interacwith the history of training Figure 1. Cognitive Maps of Physical and Social Space tions positioned each charexperience (Teki et al., 2012). The map of physical space is Cartesian and allocentric, referenced to acter along axes of power Studies on hippocampal volthe geometry of the environment and not to the individual observer. By ume do not inform us about and affiliation measured as contrast, the map of social space is polar and egocentric, referenced to the observer. the nature of hippocampal relational distance to the representation but the paralparticipant, and the combinalels between characterizations tion of relational distances along power and affiliation axes consti- to consider, however, that hippocampal of systematic mapping of multiple dimentuted a vector describing the participant’s neural activity also maps paths through sions across musical, spatial, temporal, social relationship to each character in po- space, including distinct representations and now social structure are striking. The Tavares et al. (2015) findings also lar space (Figure 1). As interactions pro- of paths that overlap in space, which ceeded in the narrative, the position of therefore measure the animal’s personal parallel evidence that the hippocampus the character moved along the coordi- experience within an allocentric frame- is essential to relational organization in nates of these two dimensions. To test work (Wood et al., 2000). Furthermore, animals and humans as they employ a their hypothesis that the hippocampus hippocampal neural activity also maps systematic mapping of relations between maps social space, Tavares et al. (2015) the temporal organization of experience, arbitrary stimuli. Early studies showed used a General Linear Model to regress independent of, or along with, movement that rats can learn a set of overlapping hippocampal activation measured in an in allocentric space, indicating that one’s stimulus associations (A is associated fMRI signal to the vector in the established sense of time is another self-generated with B; B is associated with C) that supsocial space. Their main result was that the dimension mapped by the hippocampus port inference between indirectly related fMRI signal in the left hippocampus corre- (Eichenbaum, 2014). In addition, recent stimuli (therefore A is associated with C), lated with the vector angle, indicating that evidence suggests that the spatial map indicating the existence of a cognitive the hippocampal network identified each is topological, that is, according to adja- map of a simple associative space (Buncharacter’s position in social space as cency of locations rather than reflecting sey and Eichenbaum, 1996). Hippocaman interaction of their power and affiliation the geometry of an environment (Daba- pal lesions prevent formation of this relations. Furthermore, the tracking ghian et al., 2014), suggesting that hippo- mapping in animals and, in humans perstrength for these dimensions correlated campal mapping is more about spatial forming the same task, the hippocampus with the social skills of the participant, as associations than Cartesian coordinates. activates as the associative space is assessed in a combination of question- In sum, the perspective, parameters, formed and employed (Zeithamova naires on social qualities and personality and metrics of organization in hippocam- et al., 2012). Similar reports have shown traits. pal networks seem to reflect the differing that the hippocampus is essential to the Notably, the hippocampus was not the dimensions of experience across do- mapping hierarchical relations among only brain area that mapped social mains of mapping. If there is a universal stimuli (A > B > C > D > E) in animals (Duspace, just as it is not the only brain format for relational representation in sek and Eichenbaum, 1997) and that the area that represents physical space. the hippocampus, it remains to be hippocampus is activated in the same task in humans (Heckers et al., 2004). Thus, the hippocampus is best viewed discovered. as a ‘‘hub’’ that coordinates widespread Does the hippocampus map all manner These observations strongly complement cortical areas that map different forms of spaces? The findings of Tavares et al. the findings of Tavares et al. (2015) on soof space. Also, it is notable that the map- (2015) parallel reports that the hippocam- cial space, and further extend the range of ping of egocentrically anchored social pal volume is correlated with exercise in domains in which the hippocampus supspace in the Tavares et al. (2015) study mapping and navigating auditory space ports maps of cognition. Eichenbaum and Cohen (2014) sugdiffers from the emphasis on mapping al- and medical school training. Studies locentric physical space in studies on have linked musical expertise to hippo- gested that the hippocampus supports hippocampal neuronal activity in animals campal volume (Oechslin et al., 2013). our ability to ‘‘navigate life,’’ by creating (O’Keefe and Nadel, 1978). It is important Also, Draganski et al. (2006) reported that a network of memories that permit us 10 Neuron 87, July 1, 2015 ª2015 Elsevier Inc.
Neuron
Previews to traverse new routes through an abstract memory space and solve new problems in many domains of everyday life. We suggested that memories could be related by space and time, as well as by other meaningful dimensions of experience. Consistent with this view, Tavares et al. (2015) have revealed a systematic mapping of social space by the hippocampus, complementing evidence from other approaches that support the idea that Tolman’s map of cognition applies very well to the hippocampus across domains of relational representation. REFERENCES Bunsey, M., and Eichenbaum, H. (1996). Nature 379, 255–257.
Dabaghian, Y., Brandt, V.L., and Frank, L.M. (2014). eLife 3, e03476, http://dx.doi.org/10.7554/ eLife.03476.
O’Keefe, J., and Nadel, L. (1978). The Hippocampus as a Cognitive Map (New York: Oxford University Press).
Draganski, B., Gaser, C., Kempermann, G., Kuhn, H.G., Winkler, J., Bu¨chel, C., and May, A. (2006). J. Neurosci. 26, 6314–6317.
Oechslin, M.S., Descloux, C., Croquelois, A., Chanal, J., Van De Ville, D., Lazeyras, F., and James, C.E. (2013). Hippocampus 23, 552–558.
Dusek, J.A., and Eichenbaum, H. (1997). Proc. Natl. Acad. Sci. USA 94, 7109–7114.
Tavares, R.M., Mendelsohn, A., Grossman, Y., Williams, C.H., Shapiro, M., Trope, Y., and Schiller, D. (2015). Neuron 87, this issue, 231–243.
Eichenbaum, H. (2014). Nat. Rev. Neurosci. 15, 732–744.
Teki, S., Kumar, S., von Kriegstein, K., Stewart, L., Lyness, C.R., Moore, B.C., Capleton, B., and Griffiths, T.D. (2012). J. Neurosci. 32, 12251–12257.
Eichenbaum, H., and Cohen, N.J. (2014). Neuron 83, 764–770.
Tolman, E.C. (1948). Psychol. Rev. 55, 189–208.
Hartley, T., Lever, C., Burgess, N., and O’Keefe, J. (2014). Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20120510. Heckers, S., Zalesak, M., Weiss, A.P., Ditman, T., and Titone, D. (2004). Hippocampus 14, 153–162.
Wood, E.R., Dudchenko, P.A., Robitsek, R.J., and Eichenbaum, H. (2000). Neuron 27, 623–633. Woollett, K., Glensman, J., and Maguire, E.A. (2008). Hippocampus 18, 981–984. Zeithamova, D., Dominick, A.L., and Preston, A.R. (2012). Neuron 75, 168–179.
Neuron 87, July 1, 2015 ª2015 Elsevier Inc. 11
Previews Laeng, B., Sirois, S., and Gredeba¨ck, G. (2012). Perspect. Psychol. Sci. 7, 18–27.
Polack, P.O., Friedman, J., and Golshani, P. (2013). Nat. Neurosci. 16, 1331–1339.
McGinley, M.J., David, S.V., and McCormick, D.A. (2015). Neuron 87, this issue, 179–192.
Posner, M.I., and Rothbart, M.K. (2000). Dev. Psychopathol. 12, 427–441.
Niell, C.M., and Stryker, M.P. (2010). Neuron 65, 472–479.
Poulet, J.F., and Petersen, C.C. (2008). Nature 454, 881–885.
Pinto, L., Goard, M.J., Estandian, D., Xu, M., Kwan, A.C., Lee, S.H., Harrison, T.C., Feng, G., and Dan, Y. (2013). Nat. Neurosci. 16, 1857–1863.
Reimer, J., Froudarakis, E., Cadwell, C.R., Yatsenko, D., Denfield, G.H., and Tolias, A.S. (2014). Neuron 84, 355–362.
Saleem, A.B., Ayaz, A., Jeffery, K.J., Harris, K.D., and Carandini, M. (2013). Nat. Neurosci. 16, 1864–1869. Schneider, D.M., Nelson, A., and Mooney, R. (2014). Nature 513, 189–194. Vinck, M., Batista-Brito, R., Knoblich, U., and Cardin, J.A. (2015). Neuron 86, 740–754. Yerkes, R.M., and Dodson, J. (1908). J. Comp. Neurol. Psychol. 18, 459–482.
The Hippocampus as a Cognitive Map . of Social Space Howard Eichenbaum1,* 1Center for Memory and Brain, Boston University, Boston, MA 02215, USA *Correspondence: [email protected] http://dx.doi.org/10.1016/j.neuron.2015.06.013
The traditional view of the hippocampus is that it creates a cognitive map to navigate physical space. Here, in this issue of Neuron, Tavares et al. (2015) show that the human hippocampus maps dimensions of social space, indicating a function in the service of navigating everyday life. Edward C. Tolman (Tolman, 1948) developed the notion of cognitive maps as a heuristic for understanding the complex cognitive mechanisms that guide behavior. His theory of purposeful behavior was aimed to contrast with the contemporaneous, widely accepted view that behavior is guided by stimulusresponse connections, and his experiments identified specific abilities that reflected cognition outside the scope of behavior that could be supported by stimulus-response learning. Tolman’s experiments focused on rats solving maze problems, but he did not interpret his findings narrowly as a description of navigational computations. Rather, he employed spatial learning to model aspects of goal-oriented decision-making, and he viewed a cognitive map as an organization of cognitive operations. Tolman emphasized that cognitive maps provide insights into human cognition broadly, including human social behavior. In this issue of Neuron, Tavares et al. (2015) realize Tolman’s broader view of cognitive maps by their characterization of a cognitive map of social organization in humans supported by the hippocampus.
A connection between the hippocampus and cognitive maps began with a landmark book by O’Keefe and Nadel (1978), who proposed that the hippocampus provided the neural basis of cognitive mapping. The book, and decades of experiments and theoretical work that followed, departed from Tolman’s map of cognition to instead focus on cognitive maps as psychological and neural representations of physical space, and on mechanisms within the hippocampus and associated brain areas that create geographical maps and perform navigational computations (Hartley et al., 2014). Originally, O’Keefe and Nadel (1978) extended their model to the representation of items and events in spatialtemporal context as an evolutionary advance of the human hippocampus to support its function in mapping memories, particularly as it might represent the deep structure of language. This extension of their theory clearly went beyond physical space (although only for humans) and, in doing so, acknowledged that information processing by the hippocampus can in principle be applied outside the domain of physical
space. To what non-spatial domains does it apply? Tavares et al. (2015) here reveal that cognitive maps in the hippocampus extend to social space. Social space is an excellent candidate for hippocampal representation, because it is a domain that, like physical space, is characterized by a combination of continuous dimensions. So, just as planar geography is characterized by two spatial dimensions, social space has been characterized by multiple social dimensions, including of particular relevance here, the dimensions of power and affiliation. Importantly, just as the dimensions of geographic space are defined in terms of continuous metrics of physical distance, power and affiliation are defined in terms of continuous metrics of social distance. To test the idea that social relations are mapped within the hippocampus, Tavares et al. (2015) designed a role-playing game in which participants imagined they had moved to a new town and their goal was to find a job and place to live. To accomplish this, the participants conversed with local people in the search for a job or home through different Neuron 87, July 1, 2015 ª2015 Elsevier Inc. 9
Neuron
Previews
responses in which they could hippocampal volume gray comply with a character’s dematter is increased during mand or make demands medical training, although (increasing or decreasing the Woollett et al., (2008) reported power of the character) and that medical doctors do not engage or not engage in perhave larger hippocampi, sonal conversation and physwhereas London taxi drivers ical interaction (increasing or do. Most intriguing is a report decreasing affiliation with the that professional piano tuners character), and the accumulawho spend thousands of hours tion of successive interacnavigating acoustic scenes tions took the narrative in have larger hippocampal gray different directions. The outmatter volumes associated comes of these social interacwith the history of training Figure 1. Cognitive Maps of Physical and Social Space tions positioned each charexperience (Teki et al., 2012). The map of physical space is Cartesian and allocentric, referenced to acter along axes of power Studies on hippocampal volthe geometry of the environment and not to the individual observer. By ume do not inform us about and affiliation measured as contrast, the map of social space is polar and egocentric, referenced to the observer. the nature of hippocampal relational distance to the representation but the paralparticipant, and the combinalels between characterizations tion of relational distances along power and affiliation axes consti- to consider, however, that hippocampal of systematic mapping of multiple dimentuted a vector describing the participant’s neural activity also maps paths through sions across musical, spatial, temporal, social relationship to each character in po- space, including distinct representations and now social structure are striking. The Tavares et al. (2015) findings also lar space (Figure 1). As interactions pro- of paths that overlap in space, which ceeded in the narrative, the position of therefore measure the animal’s personal parallel evidence that the hippocampus the character moved along the coordi- experience within an allocentric frame- is essential to relational organization in nates of these two dimensions. To test work (Wood et al., 2000). Furthermore, animals and humans as they employ a their hypothesis that the hippocampus hippocampal neural activity also maps systematic mapping of relations between maps social space, Tavares et al. (2015) the temporal organization of experience, arbitrary stimuli. Early studies showed used a General Linear Model to regress independent of, or along with, movement that rats can learn a set of overlapping hippocampal activation measured in an in allocentric space, indicating that one’s stimulus associations (A is associated fMRI signal to the vector in the established sense of time is another self-generated with B; B is associated with C) that supsocial space. Their main result was that the dimension mapped by the hippocampus port inference between indirectly related fMRI signal in the left hippocampus corre- (Eichenbaum, 2014). In addition, recent stimuli (therefore A is associated with C), lated with the vector angle, indicating that evidence suggests that the spatial map indicating the existence of a cognitive the hippocampal network identified each is topological, that is, according to adja- map of a simple associative space (Buncharacter’s position in social space as cency of locations rather than reflecting sey and Eichenbaum, 1996). Hippocaman interaction of their power and affiliation the geometry of an environment (Daba- pal lesions prevent formation of this relations. Furthermore, the tracking ghian et al., 2014), suggesting that hippo- mapping in animals and, in humans perstrength for these dimensions correlated campal mapping is more about spatial forming the same task, the hippocampus with the social skills of the participant, as associations than Cartesian coordinates. activates as the associative space is assessed in a combination of question- In sum, the perspective, parameters, formed and employed (Zeithamova naires on social qualities and personality and metrics of organization in hippocam- et al., 2012). Similar reports have shown traits. pal networks seem to reflect the differing that the hippocampus is essential to the Notably, the hippocampus was not the dimensions of experience across do- mapping hierarchical relations among only brain area that mapped social mains of mapping. If there is a universal stimuli (A > B > C > D > E) in animals (Duspace, just as it is not the only brain format for relational representation in sek and Eichenbaum, 1997) and that the area that represents physical space. the hippocampus, it remains to be hippocampus is activated in the same task in humans (Heckers et al., 2004). Thus, the hippocampus is best viewed discovered. as a ‘‘hub’’ that coordinates widespread Does the hippocampus map all manner These observations strongly complement cortical areas that map different forms of spaces? The findings of Tavares et al. the findings of Tavares et al. (2015) on soof space. Also, it is notable that the map- (2015) parallel reports that the hippocam- cial space, and further extend the range of ping of egocentrically anchored social pal volume is correlated with exercise in domains in which the hippocampus supspace in the Tavares et al. (2015) study mapping and navigating auditory space ports maps of cognition. Eichenbaum and Cohen (2014) sugdiffers from the emphasis on mapping al- and medical school training. Studies locentric physical space in studies on have linked musical expertise to hippo- gested that the hippocampus supports hippocampal neuronal activity in animals campal volume (Oechslin et al., 2013). our ability to ‘‘navigate life,’’ by creating (O’Keefe and Nadel, 1978). It is important Also, Draganski et al. (2006) reported that a network of memories that permit us 10 Neuron 87, July 1, 2015 ª2015 Elsevier Inc.
Neuron
Previews to traverse new routes through an abstract memory space and solve new problems in many domains of everyday life. We suggested that memories could be related by space and time, as well as by other meaningful dimensions of experience. Consistent with this view, Tavares et al. (2015) have revealed a systematic mapping of social space by the hippocampus, complementing evidence from other approaches that support the idea that Tolman’s map of cognition applies very well to the hippocampus across domains of relational representation. REFERENCES Bunsey, M., and Eichenbaum, H. (1996). Nature 379, 255–257.
Dabaghian, Y., Brandt, V.L., and Frank, L.M. (2014). eLife 3, e03476, http://dx.doi.org/10.7554/ eLife.03476.
O’Keefe, J., and Nadel, L. (1978). The Hippocampus as a Cognitive Map (New York: Oxford University Press).
Draganski, B., Gaser, C., Kempermann, G., Kuhn, H.G., Winkler, J., Bu¨chel, C., and May, A. (2006). J. Neurosci. 26, 6314–6317.
Oechslin, M.S., Descloux, C., Croquelois, A., Chanal, J., Van De Ville, D., Lazeyras, F., and James, C.E. (2013). Hippocampus 23, 552–558.
Dusek, J.A., and Eichenbaum, H. (1997). Proc. Natl. Acad. Sci. USA 94, 7109–7114.
Tavares, R.M., Mendelsohn, A., Grossman, Y., Williams, C.H., Shapiro, M., Trope, Y., and Schiller, D. (2015). Neuron 87, this issue, 231–243.
Eichenbaum, H. (2014). Nat. Rev. Neurosci. 15, 732–744.
Teki, S., Kumar, S., von Kriegstein, K., Stewart, L., Lyness, C.R., Moore, B.C., Capleton, B., and Griffiths, T.D. (2012). J. Neurosci. 32, 12251–12257.
Eichenbaum, H., and Cohen, N.J. (2014). Neuron 83, 764–770.
Tolman, E.C. (1948). Psychol. Rev. 55, 189–208.
Hartley, T., Lever, C., Burgess, N., and O’Keefe, J. (2014). Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20120510. Heckers, S., Zalesak, M., Weiss, A.P., Ditman, T., and Titone, D. (2004). Hippocampus 14, 153–162.
Wood, E.R., Dudchenko, P.A., Robitsek, R.J., and Eichenbaum, H. (2000). Neuron 27, 623–633. Woollett, K., Glensman, J., and Maguire, E.A. (2008). Hippocampus 18, 981–984. Zeithamova, D., Dominick, A.L., and Preston, A.R. (2012). Neuron 75, 168–179.
Neuron 87, July 1, 2015 ª2015 Elsevier Inc. 11
