- Email: [email protected]
Microbiology: Mixing Wine, Chocolate, and Coffee
Current Biology
Dispatches Microbiology: Mixing Wine, Chocolate, and Coffee Matthew R. Goddard The School of Life Sciences, The University of Lincoln, LN6 7DL, UK and The School of Biological Sciences, The University of Auckland, New Zealand Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2016.02.046
Yeasts associated with cocoa and coffee beans are genetically distinct. These populations have been created through the migration and mixing of populations associated with vineyards, trees in America, and the ancestral seat of this species in Far East Asia. A trip to a distant continent plainly illustrates different kinds of plants and animals are found in different parts of the world: classic oak and beech woodlands in Northern Europe, and massive Kauris mixed with cabbage trees, Rimu and Nikau palms on the North Island of New Zealand, for example. Humans’ impact on species distributions is substantial: one may also see New Zealand cabbage trees happily growing in southern English gardens, and European oak trees in New Zealand parks. Microbes are key components of natural and agricultural ecosystems, but since they, by definition, are not immediately observable, the nature of their distributions is cryptic. One microbe is of particular interest as it drives the production of bread, beer, wine, spirits, and bioethanol, and is also a research super-model: the yeast Saccharomyces cerevisiae. Even for this well studied microbe, we are still unraveling the basics of its distribution and ecology [1]. A new study by Ludlow et al. [2] reported in this issue of Current Biology shows that the S. cerevisiae (herein referred to as yeast) populations associated with cocoa and coffee beans in South America and Africa are genetically distinct, and that these various populations were founded by the migration and mixing of existing yeast populations found in other habitats and areas, which was likely facilitated by humans. Humans have moved species beyond their natural ranges for thousands of years, both intentionally for agricultural purposes and unintentionally as a consequence of human migration [3]. Other than disease agents, whose effects are apparent once transposed, the extent to which humans have
affected microbial distributions is very poorly characterized [4]. Early ideas suggested microbes have virtually limitless dispersal abilities. However, while some microbes appear globally distributed, others are certainly not [5], and the forces which give rise to these various microbial distribution patterns are not clear [6,7]. To help answer these types of questions Ludlow et al. [2] focused on what has been called the world’s most important microbe. Due to its relatively small genome and experimental pliability, this species helped develop human population genomics methods. Two parallel studies revealed a global picture for this species, which sketched a few well-defined populations, but with many individuals that were chimeras (hybrids) between different groups [8,9]. Yeast are sexual eukaryotes, and so mating between gametes (spores) deriving from genetically divergent populations to create such hybrids may easily occur. While some populations appeared to only reside in specific areas, one striking observation was that populations associated with winemaking were found in vineyards globally. This observation correlates with an earlier study showing the gross pattern and timing of genetic divergence within the wine population approximately matches the pattern for global dispersal of vines by humans [10]. It was recently shown this wine group had its origins in a population residing on Mediterranean oak trees [11]. A separate genetically distinct yeast population has also been found on oak trees in North America [12]. Lastly, a further study discovered a large and genetically diverse yeast population in forests in China, and this is likely the ancestral seat of this species [13].
Our knowledge of the habitat range and geographic distribution of S. cerevisiae is based on a relatively few samples taken from a few habitats in a few places [1]. This yeast species is also known to be associated with the processing (fermentation) of coffee and cocoa (chocolate) beans. Like vines, humans have also moved these crops around the globe: cocoa is native to the Amazon and Orinoco basins of Colombia and Venezuela, but has been taken to Africa; coffee is native to Ethiopia, but has been reciprocally moved to South America. Ludlow et al. [2] asked whether those yeasts associated with coffee and cocoa are part of the same populations as those associated with vines, and whether they show similar patterns of tracking crops as humans moved them. Ludlow et al. [2] isolated 140 strains from cocoa and coffee beans originating from various locations in Africa and South America, and also included various strains representing the previously described wine, North American oak and Chinese populations. They sequenced similar parts of the genomes of each of these strains, and compared these sequences across yeast groups. The first striking observation was that strains associated with coffee and cocoa were genetically different from the wine population, and had greater diversity. This shows the yeasts associated with cocoa and coffee are not part of the vine-associated group that has been globalized by humans. Ludlow et al. [2] went on to test the structure of these populations, which was achieved by evaluating whether there were closely related sub-groups within the data. These methods showed that the strains associated with cocoa and
Current Biology 26, R275–R296, April 4, 2016 ª2016 Elsevier Ltd All rights reserved R275
Current Biology
Dispatches
0
~190
0
~160
Current Biology
Figure 1. Global yeast migrations. Probable inferred yeast migration events (red) from the wine, North American oak and Chinese populations, to create the region-specific cocoa and coffee populations revealed by Ludlow et al. [2]. The timings of cocoa and coffee plant movements (green) between South America and Africa is also shown.
coffee comprised geographically distinct sub-populations. The accuracy of this genetic signal was not just at the continental scale; the genetic signatures were strong enough to discriminate between populations of yeasts residing on each crop in various regions within South America and Africa. Indeed, Ludlow et al. [2] show that one is able to reliably predict the origin of cocoa and coffee beans given the genetic signatures of yeasts associated with these beans. While a similar pattern has been shown for yeasts associated with vines in different regions in New Zealand [14], whether such precise patterns hold for vine-associated S. cerevisiae globally has not yet been adequately tested. These observations open up the concept that microbes might be one method to authenticate the origin or provenance of crops and food produce generally. Why we find region-specific wine, coffee and cocoa populations for this species is not clear. It might be due to chance — that certain types randomly seeded different populations in certain areas, and that subsequent microbial movement has not been rampant enough to fully-mix these populations. Or, it might be due to the actions of selection: that these various populations have adaptively diverged to the prevailing conditions in each of these areas. It is more realistically some mix of these two [7]. Next Ludlow et al. [2] asked how the coffee and cocoa bean populations were
different. Their fascinating finding was that these populations did not harbour novel types of genes (alleles), but rather different combinations of alleles already present in the North American oak, wine and Chinese populations. This implies that various components of these other populations have become combined to create the separate coffee and cocoa populations currently observed. Given that neither coffee nor cocoa are grown close to these other yeast populations, this requires inferring the migration of members of the wine, North American Oak and Chinese populations. Ludlow et al. [2] conduct some nice analyses and estimate these migration events, and this is shown in Figure 1. While the picture is not completely clear, there are some clear signals, for example 30% of the South American cocoa population migrated from the North American oak population. It is not directly demonstrated that humans are the agent of transfer, but we seem the most likely vectors given our association with these crops and the distances involved. Why S. cerevisiae is associated with these various crops in the first place is rather perplexing; in fact this species has been isolated from a range of habitats, including humans. It has been asserted that S. cerevisiae is adapted to inhabit fruits, but these and other observations make this an increasingly unattractive thesis. It has recently been suggested that S. cerevisiae is not specifically adapted to any habitat, but is a generalist [1]. The
R276 Current Biology 26, R275–R296, April 4, 2016
more places we look, the more we may discover novel S. cerevisiae populations. This study more generally illustrates the extent to which human activities may alter and manipulate the range and variability of microbial species, and create novel biodiversity through the fusion of genetically disparate populations. There is another level to consider; a microbe such as S. cerevisiae is involved in the postharvest processing of crops it is associated with: grapes and grain into wine, bread and beer; cocoa into chocolate; and coffee beans into products suitable for drinking. The appeal and popularity of these products is in part due to their aroma and flavour, which is significantly influenced by yeasts during fermentation. For wine, coffee and chocolate, further appeal and value derives from the different aroma and flavour profiles sourced from different regions of the world, encapsulated by the concept of terroir. It has recently been shown that some small but significant fraction of regionspecific wine aroma and flavour signatures may be driven by yeasts [15]. Ludlow et al.’s [2] study shows that since different yeast populations are also associated with coffee and cocoa grown in different regions, this concept might hold for other crops and their transformed produce too. REFERENCES 1. Goddard, M.R., and Greig, D. (2015). Saccharomyces cerevisiae: a nomadic yeast with no niche? FEMS Yeast Res. 15, fov009. 2. Ludlow, C.L., Cromie, G.A., GarmendiaTorres, C., Sirr, A., Hays, M., Field, C., Jeffery, E.W., Fay, J.C., and Dudley, A.M. (2016). Independent origins of yeast associated with coffee and cacao fermentation. Curr. Biol. 26, 965–971. 3. Diamond, J. (2002). Evolution, consequences and future of plant and animal domestication. Nature 418, 700–707. 4. Litchman, E. (2010). Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems. Ecol. Lett. 13, 1560–1572. 5. Martiny, J.B.H., Bohannan, B.J.M., Brown, J.H., Colwell, R.K., Fuhrman, J.A., Green, J.L., Horner-Devine, M.C., Kane, M., Krumins, J.A., Kuske, C.R., et al. (2006). Microbial biogeography: putting microorganisms on the map. Nat. Rev. Microbiol. 4, 102–112.
Current Biology
Dispatches 6. Hanson, C.A., Fuhrman, J.A., Horner-Devine, M.C., and Martiny, J.B.H. (2012). Beyond biogeographic patterns: processes shaping the microbial landscape. Nat. Rev. Microbiol. 10, 497–506. 7. Morrison-Whittle, P., and Goddard, M.R. (2015). Quantifying the relative roles of selective and neutral processes in defining eukaryotic microbial communities. ISME J. 9, 2003–2011. 8. Liti, G., Carter, D.M., Moses, A.M., Warringer, J., Parts, L., James, S.A., Davey, R.P., Roberts, I.N., Burt, A., Koufopanou, V., et al. (2009). Population genomics of domestic and wild yeasts. Nature 458, 337–341. 9. Schacherer, J., Shapiro, J.A., Ruderfer, D.M., and Kruglyak, L. (2009). Comprehensive
polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458, 342–345. 10. Legras, J.L., Merdinoglu, D., Cornuet, J.M., and Karst, F. (2007). Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history. Mol. Ecol. 16, 2091–2102. 11. Almeida, P., Barbosa, R., Zalar, P., Imanishi, Y., Shimizu, K., Turchetti, B., Legras, J.L., Serra, M., Dequin, S., Couloux, A., et al. (2015). A population genomics insight into the Mediterranean origins of wine yeast domestication. Mol. Ecol. 24, 5412–5427. 12. Cromie, G.A., Hyma, K.E., Ludlow, C.L., Garmendia-Torres, C., Gilbert, T.L., May, P., Huang, A.A., Dudley, A.M., and Fay, J.C. (2013). Genomic sequence diversity and
population structure of Saccharomyces cerevisiae assessed by RAD-seq. G3 3, 2163–2171. 13. Wang, Q.M., Liu, W.Q., Liti, G., Wang, S.A., and Bai, F.Y. (2012). Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity. Mol. Ecol. 21, 5404–5417. 14. Knight, S.J., and Goddard, M.R. (2015). Quantifying separation and similarity in a Saccharomyces cerevisiae metapopulation. ISME J. 9, 361–370. 15. Knight, S., Klaere, S., Fedrizzi, B., and Goddard, M.R. (2015). Regional microbial signatures positively correlate with differential wine phenotypes: evidence for a microbial aspect to terroir. Sci. Rep. 5, 14233.
Spatial Cognition: Grid Cells Support Imagined Navigation Joshua Jacobs1 and Sang Ah Lee1,2 1Department
of Biomedical Engineering, Columbia University, 1210 Amsterdam Avenue, New York, NY 10027, USA of Trento Center for Mind/Brain Sciences, Corso Bettini, 31, University of Trento, 38068, Rovereto, Italy Correspondence: [email protected] (J.J.), [email protected] (S.A.L.) http://dx.doi.org/10.1016/j.cub.2016.02.032 2University
Grid cells in the entorhinal cortex represent an animal’s current location during navigation. A new study indicates that grid cells in humans also represent information about imagined movement and spatial orienting, suggesting that the entorhinal network has a flexible role in spatial representation. The network of grid cells in the entorhinal cortex (EC) appears to play a key role in how animals navigate. The activity of each grid cell provides information about the animal’s current location by spiking when the animal is present within a set of positions that form a regularly spaced grid across an environment. A new study by Horner et al. [1] reported recently in Current Biology provides striking evidence that grid cells also support other types of spatial processing, most notably imagined movement and orientation. These results imply that entorhinal grid cells support a flexible neuronal code for space that can be dynamically targeted according to thoughts and mental simulations. Grid Cells in Humans Grid cells were first discovered in rodents by recording neuronal activity as animals ran through laboratory arenas [2]. The
discovery of grid cells was an important advance in understanding how the brain supports navigation, not only because these cells reliably signal the animal’s current location but also because the regular spacing of each cell’s activity across the environment was evidence of a metric code for space that could theoretically support various types of spatial cognition [3]. For obvious ethical reasons it is challenging to record directly from individual grid cells in humans. In fact, the first evidence for grid cells in humans came from a cleverly designed functional magnetic resonance imaging (fMRI) study by some of the authors of the current paper [4]. Grid cells have several attributes that allow them to be observed with fMRI in spite of this method’s lack of resolution at the single-neuron level. First, each grid cell represents space via a triangular grid that has six-way (60 )
rotational symmetry. Second, each grid cell fires at a higher mean firing rate when the animal travels in a direction that is aligned to its grid versus a misaligned direction. Third, multiple neighboring grid cells in one individual generally represent grids with the same orientation. As a result of these attributes, Doeller et al. [4] expected the activity of grid cells to be visible in fMRI as sites that exhibited increased fMRI activity when a person moved in any of six directions that were spaced at 60 intervals (six-way rotational symmetry). Doeller et al. [4] tested this approach by having subjects perform a virtual-reality navigation task during fMRI scanning. Consistent with predictions, the fMRI response from the EC was modulated to a person’s current heading in a manner that exhibited six-way rotational symmetry. The presence of six-way symmetric fMRI heading
Current Biology 26, R275–R296, April 4, 2016 R277
Dispatches Microbiology: Mixing Wine, Chocolate, and Coffee Matthew R. Goddard The School of Life Sciences, The University of Lincoln, LN6 7DL, UK and The School of Biological Sciences, The University of Auckland, New Zealand Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2016.02.046
Yeasts associated with cocoa and coffee beans are genetically distinct. These populations have been created through the migration and mixing of populations associated with vineyards, trees in America, and the ancestral seat of this species in Far East Asia. A trip to a distant continent plainly illustrates different kinds of plants and animals are found in different parts of the world: classic oak and beech woodlands in Northern Europe, and massive Kauris mixed with cabbage trees, Rimu and Nikau palms on the North Island of New Zealand, for example. Humans’ impact on species distributions is substantial: one may also see New Zealand cabbage trees happily growing in southern English gardens, and European oak trees in New Zealand parks. Microbes are key components of natural and agricultural ecosystems, but since they, by definition, are not immediately observable, the nature of their distributions is cryptic. One microbe is of particular interest as it drives the production of bread, beer, wine, spirits, and bioethanol, and is also a research super-model: the yeast Saccharomyces cerevisiae. Even for this well studied microbe, we are still unraveling the basics of its distribution and ecology [1]. A new study by Ludlow et al. [2] reported in this issue of Current Biology shows that the S. cerevisiae (herein referred to as yeast) populations associated with cocoa and coffee beans in South America and Africa are genetically distinct, and that these various populations were founded by the migration and mixing of existing yeast populations found in other habitats and areas, which was likely facilitated by humans. Humans have moved species beyond their natural ranges for thousands of years, both intentionally for agricultural purposes and unintentionally as a consequence of human migration [3]. Other than disease agents, whose effects are apparent once transposed, the extent to which humans have
affected microbial distributions is very poorly characterized [4]. Early ideas suggested microbes have virtually limitless dispersal abilities. However, while some microbes appear globally distributed, others are certainly not [5], and the forces which give rise to these various microbial distribution patterns are not clear [6,7]. To help answer these types of questions Ludlow et al. [2] focused on what has been called the world’s most important microbe. Due to its relatively small genome and experimental pliability, this species helped develop human population genomics methods. Two parallel studies revealed a global picture for this species, which sketched a few well-defined populations, but with many individuals that were chimeras (hybrids) between different groups [8,9]. Yeast are sexual eukaryotes, and so mating between gametes (spores) deriving from genetically divergent populations to create such hybrids may easily occur. While some populations appeared to only reside in specific areas, one striking observation was that populations associated with winemaking were found in vineyards globally. This observation correlates with an earlier study showing the gross pattern and timing of genetic divergence within the wine population approximately matches the pattern for global dispersal of vines by humans [10]. It was recently shown this wine group had its origins in a population residing on Mediterranean oak trees [11]. A separate genetically distinct yeast population has also been found on oak trees in North America [12]. Lastly, a further study discovered a large and genetically diverse yeast population in forests in China, and this is likely the ancestral seat of this species [13].
Our knowledge of the habitat range and geographic distribution of S. cerevisiae is based on a relatively few samples taken from a few habitats in a few places [1]. This yeast species is also known to be associated with the processing (fermentation) of coffee and cocoa (chocolate) beans. Like vines, humans have also moved these crops around the globe: cocoa is native to the Amazon and Orinoco basins of Colombia and Venezuela, but has been taken to Africa; coffee is native to Ethiopia, but has been reciprocally moved to South America. Ludlow et al. [2] asked whether those yeasts associated with coffee and cocoa are part of the same populations as those associated with vines, and whether they show similar patterns of tracking crops as humans moved them. Ludlow et al. [2] isolated 140 strains from cocoa and coffee beans originating from various locations in Africa and South America, and also included various strains representing the previously described wine, North American oak and Chinese populations. They sequenced similar parts of the genomes of each of these strains, and compared these sequences across yeast groups. The first striking observation was that strains associated with coffee and cocoa were genetically different from the wine population, and had greater diversity. This shows the yeasts associated with cocoa and coffee are not part of the vine-associated group that has been globalized by humans. Ludlow et al. [2] went on to test the structure of these populations, which was achieved by evaluating whether there were closely related sub-groups within the data. These methods showed that the strains associated with cocoa and
Current Biology 26, R275–R296, April 4, 2016 ª2016 Elsevier Ltd All rights reserved R275
Current Biology
Dispatches
0
~190
0
~160
Current Biology
Figure 1. Global yeast migrations. Probable inferred yeast migration events (red) from the wine, North American oak and Chinese populations, to create the region-specific cocoa and coffee populations revealed by Ludlow et al. [2]. The timings of cocoa and coffee plant movements (green) between South America and Africa is also shown.
coffee comprised geographically distinct sub-populations. The accuracy of this genetic signal was not just at the continental scale; the genetic signatures were strong enough to discriminate between populations of yeasts residing on each crop in various regions within South America and Africa. Indeed, Ludlow et al. [2] show that one is able to reliably predict the origin of cocoa and coffee beans given the genetic signatures of yeasts associated with these beans. While a similar pattern has been shown for yeasts associated with vines in different regions in New Zealand [14], whether such precise patterns hold for vine-associated S. cerevisiae globally has not yet been adequately tested. These observations open up the concept that microbes might be one method to authenticate the origin or provenance of crops and food produce generally. Why we find region-specific wine, coffee and cocoa populations for this species is not clear. It might be due to chance — that certain types randomly seeded different populations in certain areas, and that subsequent microbial movement has not been rampant enough to fully-mix these populations. Or, it might be due to the actions of selection: that these various populations have adaptively diverged to the prevailing conditions in each of these areas. It is more realistically some mix of these two [7]. Next Ludlow et al. [2] asked how the coffee and cocoa bean populations were
different. Their fascinating finding was that these populations did not harbour novel types of genes (alleles), but rather different combinations of alleles already present in the North American oak, wine and Chinese populations. This implies that various components of these other populations have become combined to create the separate coffee and cocoa populations currently observed. Given that neither coffee nor cocoa are grown close to these other yeast populations, this requires inferring the migration of members of the wine, North American Oak and Chinese populations. Ludlow et al. [2] conduct some nice analyses and estimate these migration events, and this is shown in Figure 1. While the picture is not completely clear, there are some clear signals, for example 30% of the South American cocoa population migrated from the North American oak population. It is not directly demonstrated that humans are the agent of transfer, but we seem the most likely vectors given our association with these crops and the distances involved. Why S. cerevisiae is associated with these various crops in the first place is rather perplexing; in fact this species has been isolated from a range of habitats, including humans. It has been asserted that S. cerevisiae is adapted to inhabit fruits, but these and other observations make this an increasingly unattractive thesis. It has recently been suggested that S. cerevisiae is not specifically adapted to any habitat, but is a generalist [1]. The
R276 Current Biology 26, R275–R296, April 4, 2016
more places we look, the more we may discover novel S. cerevisiae populations. This study more generally illustrates the extent to which human activities may alter and manipulate the range and variability of microbial species, and create novel biodiversity through the fusion of genetically disparate populations. There is another level to consider; a microbe such as S. cerevisiae is involved in the postharvest processing of crops it is associated with: grapes and grain into wine, bread and beer; cocoa into chocolate; and coffee beans into products suitable for drinking. The appeal and popularity of these products is in part due to their aroma and flavour, which is significantly influenced by yeasts during fermentation. For wine, coffee and chocolate, further appeal and value derives from the different aroma and flavour profiles sourced from different regions of the world, encapsulated by the concept of terroir. It has recently been shown that some small but significant fraction of regionspecific wine aroma and flavour signatures may be driven by yeasts [15]. Ludlow et al.’s [2] study shows that since different yeast populations are also associated with coffee and cocoa grown in different regions, this concept might hold for other crops and their transformed produce too. REFERENCES 1. Goddard, M.R., and Greig, D. (2015). Saccharomyces cerevisiae: a nomadic yeast with no niche? FEMS Yeast Res. 15, fov009. 2. Ludlow, C.L., Cromie, G.A., GarmendiaTorres, C., Sirr, A., Hays, M., Field, C., Jeffery, E.W., Fay, J.C., and Dudley, A.M. (2016). Independent origins of yeast associated with coffee and cacao fermentation. Curr. Biol. 26, 965–971. 3. Diamond, J. (2002). Evolution, consequences and future of plant and animal domestication. Nature 418, 700–707. 4. Litchman, E. (2010). Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems. Ecol. Lett. 13, 1560–1572. 5. Martiny, J.B.H., Bohannan, B.J.M., Brown, J.H., Colwell, R.K., Fuhrman, J.A., Green, J.L., Horner-Devine, M.C., Kane, M., Krumins, J.A., Kuske, C.R., et al. (2006). Microbial biogeography: putting microorganisms on the map. Nat. Rev. Microbiol. 4, 102–112.
Current Biology
Dispatches 6. Hanson, C.A., Fuhrman, J.A., Horner-Devine, M.C., and Martiny, J.B.H. (2012). Beyond biogeographic patterns: processes shaping the microbial landscape. Nat. Rev. Microbiol. 10, 497–506. 7. Morrison-Whittle, P., and Goddard, M.R. (2015). Quantifying the relative roles of selective and neutral processes in defining eukaryotic microbial communities. ISME J. 9, 2003–2011. 8. Liti, G., Carter, D.M., Moses, A.M., Warringer, J., Parts, L., James, S.A., Davey, R.P., Roberts, I.N., Burt, A., Koufopanou, V., et al. (2009). Population genomics of domestic and wild yeasts. Nature 458, 337–341. 9. Schacherer, J., Shapiro, J.A., Ruderfer, D.M., and Kruglyak, L. (2009). Comprehensive
polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458, 342–345. 10. Legras, J.L., Merdinoglu, D., Cornuet, J.M., and Karst, F. (2007). Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history. Mol. Ecol. 16, 2091–2102. 11. Almeida, P., Barbosa, R., Zalar, P., Imanishi, Y., Shimizu, K., Turchetti, B., Legras, J.L., Serra, M., Dequin, S., Couloux, A., et al. (2015). A population genomics insight into the Mediterranean origins of wine yeast domestication. Mol. Ecol. 24, 5412–5427. 12. Cromie, G.A., Hyma, K.E., Ludlow, C.L., Garmendia-Torres, C., Gilbert, T.L., May, P., Huang, A.A., Dudley, A.M., and Fay, J.C. (2013). Genomic sequence diversity and
population structure of Saccharomyces cerevisiae assessed by RAD-seq. G3 3, 2163–2171. 13. Wang, Q.M., Liu, W.Q., Liti, G., Wang, S.A., and Bai, F.Y. (2012). Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity. Mol. Ecol. 21, 5404–5417. 14. Knight, S.J., and Goddard, M.R. (2015). Quantifying separation and similarity in a Saccharomyces cerevisiae metapopulation. ISME J. 9, 361–370. 15. Knight, S., Klaere, S., Fedrizzi, B., and Goddard, M.R. (2015). Regional microbial signatures positively correlate with differential wine phenotypes: evidence for a microbial aspect to terroir. Sci. Rep. 5, 14233.
Spatial Cognition: Grid Cells Support Imagined Navigation Joshua Jacobs1 and Sang Ah Lee1,2 1Department
of Biomedical Engineering, Columbia University, 1210 Amsterdam Avenue, New York, NY 10027, USA of Trento Center for Mind/Brain Sciences, Corso Bettini, 31, University of Trento, 38068, Rovereto, Italy Correspondence: [email protected] (J.J.), [email protected] (S.A.L.) http://dx.doi.org/10.1016/j.cub.2016.02.032 2University
Grid cells in the entorhinal cortex represent an animal’s current location during navigation. A new study indicates that grid cells in humans also represent information about imagined movement and spatial orienting, suggesting that the entorhinal network has a flexible role in spatial representation. The network of grid cells in the entorhinal cortex (EC) appears to play a key role in how animals navigate. The activity of each grid cell provides information about the animal’s current location by spiking when the animal is present within a set of positions that form a regularly spaced grid across an environment. A new study by Horner et al. [1] reported recently in Current Biology provides striking evidence that grid cells also support other types of spatial processing, most notably imagined movement and orientation. These results imply that entorhinal grid cells support a flexible neuronal code for space that can be dynamically targeted according to thoughts and mental simulations. Grid Cells in Humans Grid cells were first discovered in rodents by recording neuronal activity as animals ran through laboratory arenas [2]. The
discovery of grid cells was an important advance in understanding how the brain supports navigation, not only because these cells reliably signal the animal’s current location but also because the regular spacing of each cell’s activity across the environment was evidence of a metric code for space that could theoretically support various types of spatial cognition [3]. For obvious ethical reasons it is challenging to record directly from individual grid cells in humans. In fact, the first evidence for grid cells in humans came from a cleverly designed functional magnetic resonance imaging (fMRI) study by some of the authors of the current paper [4]. Grid cells have several attributes that allow them to be observed with fMRI in spite of this method’s lack of resolution at the single-neuron level. First, each grid cell represents space via a triangular grid that has six-way (60 )
rotational symmetry. Second, each grid cell fires at a higher mean firing rate when the animal travels in a direction that is aligned to its grid versus a misaligned direction. Third, multiple neighboring grid cells in one individual generally represent grids with the same orientation. As a result of these attributes, Doeller et al. [4] expected the activity of grid cells to be visible in fMRI as sites that exhibited increased fMRI activity when a person moved in any of six directions that were spaced at 60 intervals (six-way rotational symmetry). Doeller et al. [4] tested this approach by having subjects perform a virtual-reality navigation task during fMRI scanning. Consistent with predictions, the fMRI response from the EC was modulated to a person’s current heading in a manner that exhibited six-way rotational symmetry. The presence of six-way symmetric fMRI heading
Current Biology 26, R275–R296, April 4, 2016 R277