The Hippocampus as a Cognitive Map … of Social Space
2015; Cell Press; Volume: 87; Issue: 1 Linguagem: Inglês
10.1016/j.neuron.2015.06.013
ISSN1097-4199
Autores Tópico(s)Child and Animal Learning Development
ResumoThe 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., 2015Tavares R.M. Mendelsohn A. Grossman Y. Williams C.H. Shapiro M. Trope Y. Schiller D. Neuron. 2015; 87 (this issue): 231-243Abstract Full Text Full Text PDF PubMed Scopus (209) Google Scholar show that the human hippocampus maps dimensions of social space, indicating a function in the service of navigating everyday life. 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., 2015Tavares R.M. Mendelsohn A. Grossman Y. Williams C.H. Shapiro M. Trope Y. Schiller D. Neuron. 2015; 87 (this issue): 231-243Abstract Full Text Full Text PDF PubMed Scopus (209) Google Scholar show that the human hippocampus maps dimensions of social space, indicating a function in the service of navigating everyday life. Edward C. Tolman (Tolman, 1948Tolman E.C. Psychol. Rev. 1948; 55: 189-208Crossref PubMed Scopus (3685) Google Scholar) 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 stimulus-response 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., 2015Tavares R.M. Mendelsohn A. Grossman Y. Williams C.H. Shapiro M. Trope Y. Schiller D. Neuron. 2015; 87 (this issue): 231-243Abstract Full Text Full Text PDF PubMed Scopus (209) Google Scholar 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, 1978O'Keefe J. Nadel L. The Hippocampus as a Cognitive Map. Oxford University Press, New York1978Google Scholar, 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., 2014Hartley T. Lever C. Burgess N. O'Keefe J. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014; 369: 20120510Crossref PubMed Scopus (293) Google Scholar). Originally, O'Keefe and Nadel, 1978O'Keefe J. Nadel L. The Hippocampus as a Cognitive Map. Oxford University Press, New York1978Google Scholar extended their model to the representation of items and events in spatial-temporal 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., 2015Tavares R.M. Mendelsohn A. Grossman Y. Williams C.H. Shapiro M. Trope Y. Schiller D. Neuron. 2015; 87 (this issue): 231-243Abstract Full Text Full Text PDF PubMed Scopus (209) Google Scholar 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., 2015Tavares R.M. Mendelsohn A. Grossman Y. Williams C.H. Shapiro M. Trope Y. Schiller D. Neuron. 2015; 87 (this issue): 231-243Abstract Full Text Full Text PDF PubMed Scopus (209) Google Scholar 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 responses in which they could comply with a character's demand or make demands (increasing or decreasing the power of the character) and engage or not engage in personal conversation and physical interaction (increasing or decreasing affiliation with the character), and the accumulation of successive interactions took the narrative in different directions. The outcomes of these social interactions positioned each character along axes of power and affiliation measured as relational distance to the participant, and the combination of relational distances along power and affiliation axes constituted a vector describing the participant's social relationship to each character in polar space (Figure 1). As interactions proceeded in the narrative, the position of the character moved along the coordinates of these two dimensions. To test their hypothesis that the hippocampus maps social space, Tavares et al., 2015Tavares R.M. Mendelsohn A. Grossman Y. Williams C.H. Shapiro M. Trope Y. Schiller D. Neuron. 2015; 87 (this issue): 231-243Abstract Full Text Full Text PDF PubMed Scopus (209) Google Scholar used a General Linear Model to regress hippocampal activation measured in an fMRI signal to the vector in the established social space. Their main result was that the fMRI signal in the left hippocampus correlated with the vector angle, indicating that the hippocampal network identified each character's position in social space as an interaction of their power and affiliation relations. Furthermore, the tracking strength for these dimensions correlated with the social skills of the participant, as assessed in a combination of questionnaires on social qualities and personality traits. Notably, the hippocampus was not the only brain area that mapped social space, just as it is not the only brain area that represents physical space. Thus, the hippocampus is best viewed as a "hub" that coordinates widespread cortical areas that map different forms of space. Also, it is notable that the mapping of egocentrically anchored social space in the Tavares et al., 2015Tavares R.M. Mendelsohn A. Grossman Y. Williams C.H. Shapiro M. Trope Y. Schiller D. Neuron. 2015; 87 (this issue): 231-243Abstract Full Text Full Text PDF PubMed Scopus (209) Google Scholar study differs from the emphasis on mapping allocentric physical space in studies on hippocampal neuronal activity in animals (O'Keefe and Nadel, 1978O'Keefe J. Nadel L. The Hippocampus as a Cognitive Map. Oxford University Press, New York1978Google Scholar). It is important to consider, however, that hippocampal neural activity also maps paths through space, including distinct representations of paths that overlap in space, which therefore measure the animal's personal experience within an allocentric framework (Wood et al., 2000Wood E.R. Dudchenko P.A. Robitsek R.J. Eichenbaum H. Neuron. 2000; 27: 623-633Abstract Full Text Full Text PDF PubMed Scopus (652) Google Scholar). Furthermore, hippocampal neural activity also maps the temporal organization of experience, independent of, or along with, movement in allocentric space, indicating that one's sense of time is another self-generated dimension mapped by the hippocampus (Eichenbaum, 2014Eichenbaum H. Nat. Rev. Neurosci. 2014; 15: 732-744Crossref PubMed Scopus (387) Google Scholar). In addition, recent evidence suggests that the spatial map is topological, that is, according to adjacency of locations rather than reflecting the geometry of an environment (Dabaghian et al., 2014Dabaghian Y. Brandt V.L. Frank L.M. eLife. 2014; 3: e03476https://doi.org/10.7554/eLife.03476Crossref Scopus (74) Google Scholar), suggesting that hippocampal mapping is more about spatial associations than Cartesian coordinates. In sum, the perspective, parameters, and metrics of organization in hippocampal networks seem to reflect the differing dimensions of experience across domains of mapping. If there is a universal format for relational representation in the hippocampus, it remains to be discovered. Does the hippocampus map all manner of spaces? The findings of Tavares et al., 2015Tavares R.M. Mendelsohn A. Grossman Y. Williams C.H. Shapiro M. Trope Y. Schiller D. Neuron. 2015; 87 (this issue): 231-243Abstract Full Text Full Text PDF PubMed Scopus (209) Google Scholar parallel reports that the hippocampal volume is correlated with exercise in mapping and navigating auditory space and medical school training. Studies have linked musical expertise to hippocampal volume (Oechslin et al., 2013Oechslin M.S. Descloux C. Croquelois A. Chanal J. Van De Ville D. Lazeyras F. James C.E. Hippocampus. 2013; 23: 552-558Crossref PubMed Scopus (24) Google Scholar). Also, Draganski et al., 2006Draganski B. Gaser C. Kempermann G. Kuhn H.G. Winkler J. Büchel C. May A. J. Neurosci. 2006; 26: 6314-6317Crossref PubMed Scopus (530) Google Scholar reported that hippocampal volume gray matter is increased during medical training, although Woollett et al., 2008Woollett K. Glensman J. Maguire E.A. Hippocampus. 2008; 18: 981-984Crossref PubMed Scopus (15) Google Scholar reported that medical doctors do not have larger hippocampi, whereas London taxi drivers do. Most intriguing is a report that professional piano tuners who spend thousands of hours navigating acoustic scenes have larger hippocampal gray matter volumes associated with the history of training experience (Teki et al., 2012Teki S. Kumar S. von Kriegstein K. Stewart L. Lyness C.R. Moore B.C. Capleton B. Griffiths T.D. J. Neurosci. 2012; 32: 12251-12257Crossref PubMed Scopus (34) Google Scholar). Studies on hippocampal volume do not inform us about the nature of hippocampal representation but the parallels between characterizations of systematic mapping of multiple dimensions across musical, spatial, temporal, and now social structure are striking. The Tavares et al., 2015Tavares R.M. Mendelsohn A. Grossman Y. Williams C.H. Shapiro M. Trope Y. Schiller D. Neuron. 2015; 87 (this issue): 231-243Abstract Full Text Full Text PDF PubMed Scopus (209) Google Scholar findings also parallel evidence that the hippocampus is essential to relational organization in animals and humans as they employ a systematic mapping of relations between arbitrary stimuli. Early studies showed that rats can learn a set of overlapping stimulus associations (A is associated with B; B is associated with C) that support inference between indirectly related stimuli (therefore A is associated with C), indicating the existence of a cognitive map of a simple associative space (Bunsey and Eichenbaum, 1996Bunsey M. Eichenbaum H. Nature. 1996; 379: 255-257Crossref PubMed Scopus (514) Google Scholar). Hippocampal lesions prevent formation of this mapping in animals and, in humans performing the same task, the hippocampus activates as the associative space is formed and employed (Zeithamova et al., 2012Zeithamova D. Dominick A.L. Preston A.R. Neuron. 2012; 75: 168-179Abstract Full Text Full Text PDF PubMed Scopus (324) Google Scholar). Similar reports have shown that the hippocampus is essential to the mapping hierarchical relations among stimuli (A > B > C > D > E) in animals (Dusek and Eichenbaum, 1997Dusek J.A. Eichenbaum H. Proc. Natl. Acad. Sci. USA. 1997; 94: 7109-7114Crossref PubMed Scopus (424) Google Scholar) and that the hippocampus is activated in the same task in humans (Heckers et al., 2004Heckers S. Zalesak M. Weiss A.P. Ditman T. Titone D. Hippocampus. 2004; 14: 153-162Crossref PubMed Scopus (221) Google Scholar). These observations strongly complement the findings of Tavares et al., 2015Tavares R.M. Mendelsohn A. Grossman Y. Williams C.H. Shapiro M. Trope Y. Schiller D. Neuron. 2015; 87 (this issue): 231-243Abstract Full Text Full Text PDF PubMed Scopus (209) Google Scholar on social space, and further extend the range of domains in which the hippocampus supports maps of cognition. Eichenbaum and Cohen, 2014Eichenbaum H. Cohen N.J. Neuron. 2014; 83: 764-770Abstract Full Text Full Text PDF PubMed Scopus (336) Google Scholar suggested that the hippocampus supports our ability to "navigate life," by creating a network of memories that permit us 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., 2015Tavares R.M. Mendelsohn A. Grossman Y. Williams C.H. Shapiro M. Trope Y. Schiller D. Neuron. 2015; 87 (this issue): 231-243Abstract Full Text Full Text PDF PubMed Scopus (209) Google Scholar 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. A Map for Social Navigation in the Human BrainTavares et al.NeuronJuly 01, 2015In BriefHow do we navigate social relationships? Tavares et al. found that when people interacted with others in a virtual neighborhood, hippocampal activity correlated with movement through an abstract, two-dimensional social space framed by power and affiliation: a social cognitive map. Full-Text PDF Open Archive
Referência(s)