- Email: [email protected]
Spatial Navigation: Retrosplenial Cortex Encodes the Spatial Structure of Complex Routes
Current Biology
Dispatches 2. Fry, B.G., Roelants, K., Champagne, D.E., Scheib, H., Tyndall, J.D.A., King, G.F., Nevalainen, T.J., Norman, J.A., Lewis, R.J., Norton, R.S., et al. (2009). The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu. Rev. Genomics. Hum. Genet. 10, 483–511. 3. Chang, D., and Duda, T.F. (2012). Extensive and continuous duplication facilitates rapid evolution and diversification of gene families. Mol. Biol. Evol. 29, 2019–2029.
patterns of platypus defensin and related venom genes across a range of tissue types reveal the possibility of broader functions for OvDLPs than previously suspected. Toxicon 52, 559–565. 9. Hargreaves, A.D., Swain, M.T., Hegarty, M.J., Logan, D.W., and Mulley, J.F. (2014). Restriction and recruitment-gene duplication and the origin and evolution of snake venom toxins. Genome Biol. Evol. 6, 2088– 2095.
4. Vonk, F.J., Casewell, N.R., Henkel, C.V., Heimberg, A.M., Jansen, H.J., McCleary, R.J.R., Kerkkamp, H.M., Vos, R.A., Guerreiro, I., Calvete, J.J., et al. (2013). The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. Proc. Natl. Acad. Sci. USA 110, 20651–20656.
10. Junqueira-de-Azevedo, I.L.M., Bastos, C.M.V., Ho, P.L., Luna, M.S., Yamanouye, N., and Casewell, N.R. (2015). Venom-related transcripts from Bothrops jararaca tissues provide novel molecular insights into the production and evolution of snake venom. Mol. Biol. Evol. 32, 754–766.
5. Sanggaard, K.W., Bechsgaard, J.S., Fang, X., Duan, J., Dyrlund, T.F., Gupta, V., Jiang, X., Cheng, L., Fan, D., Feng, Y., et al. (2014). Spider genomes provide insight into composition and evolution of venom and silk. Nat. Commun. 5, 3765.
11. Reyes-Velasco, J., Card, D.C., Andrew, A.L., Shaney, K.J., Adams, R.H., Schield, D.R., Casewell, N.R., Mackessy, S.P., and Castoe, T.A. (2015). Expression of venom gene homologs in diverse python tissues suggests a new model for the evolution of snake venom. Mol. Biol. Evol. 32, 173–183.
6. Martinson, E., Mrinalini, Kelkar, Y.D., Chang, C.-H., and Werren, J.H. (2017). The evolution of venom by co-option of single copy genes. Curr. Biol. 27, 2007–2013. 7. Wang, X., Gao, B., and Zhu, S. (2016). Exon shuffling and origin of scorpion venom biodiversity. Toxins (Basel) 9, 10.
12. Margres, M.J., Bigelow, A.T., Lemmon, E.M., Lemmon, A.R., and Rokyta, D.R. (2017). Selection to increase expression, not sequence diversity, precedes gene family origin and expansion in rattlesnake venom. Genetics. http://dx.doi.org/10.1534/genetics. 117.202655.
8. Whittington, C.M., Papenfuss, A.T., Kuchel, P.W., and Belov, K. (2008). Expression
13. Nei, M., Gu, X., and Sitnikova, T. (1997). Evolution by the birth-and-death process in
multigene families of the vertebrate immune system. Proc. Natl. Acad. Sci. USA 94, 7799– 7806. 14. Sunagar, K., Moran, Y., Salemi, M., Chen, L., Wang, Y., and Pond, S.K. (2015). The rise and fall of an evolutionary innovation: contrasting strategies of venom evolution in ancient and young animals. PLOS Genet. 11, e1005596. 15. Terlau, H., and Olivera, B.M. (2004). Conus venoms: a rich source of novel ion channeltargeted peptides. Physiol. Rev. 84, 41–68. 16. Martinson, E.O., Wheeler, D., Wright, J., Mrinalini, Siebert, A.L., and Werren, J.H. (2014). Nasonia vitripennis venom causes targeted gene expression changes in its fly host. Mol. Ecol. 23, 5918–5930. 17. Mrinalini, Siebert, A.L., Wright, J., Martinson, E., Wheeler, D., and Werren, J.H. (2015). Parasitoid venom induces metabolic cascades in fly hosts. Metabolomics 11, 350–366. 18. Wong, E.S.W., Papenfuss, A.T., Whittington, C.M., Warren, W.C., and Belov, K. (2012). A limited role for gene duplications in the evolution of platypus venom. Mol. Biol. Evol. 29, 167–177. 19. Conant, G.C., and Wolfe, K.H. (2008). Turning a hobby into a job: how duplicated genes find new functions. Nat. Rev. Genet. 9, 938–950. 20. Smith, C.W., and Valca´rcel, J. (2000). Alternative pre-mRNA splicing: the logic of combinatorial control. Trends Biochem. Sci. 25, 381–388.
Spatial Navigation: Retrosplenial Cortex Encodes the Spatial Structure of Complex Routes Benjamin J. Clark Department of Psychology, University of New Mexico, MSC03 2220, 1 University of New Mexico, Albuquerque, NM 87131, USA Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2017.05.019
A new study in which recordings were made from the retrosplenial cortex while rats navigated through a complex environment has revealed populations of cells that encode route-segments as well as the relative position of these segments within an allocentric framework. There is considerable evidence that animals, including humans, can navigate by referencing the geometric contours and cues defining a local environment, while at the same time monitoring their position and direction in relation to a global or allocentric framework [1,2]. The capacity to make use of both local and global frames of reference allows for ease in navigation in which subjects may
rapidly alter their sequence of movements, or their route, towards a goal. These can involve a large-scale modification in the structure of the route, or a mere update to a small segment of the path. Flexible changes in route structure suggest that animals may retain information regarding the action patterns that make up a route, while at
the same time keeping track of the relationships between the various routesegments. The mechanisms by which route structure is processed at local and global spatial scales are poorly understood, but work published recently in Current Biology by Alexander and Nitz [3] suggests a role for neurons in the retrosplenial cortex, a dorsal cortical structure that occupies a pivotal
Current Biology 27, R642–R666, July 10, 2017 ª 2017 Elsevier Ltd. R649
Current Biology
Dispatches position between posterior sensory and limbic-hippocampal systems, and that has been linked to integrative functions such as spatial navigation and memory [4–6]. A number of previous observations have indicated that retrosplenial cortex may be involved in route planning. Firstly, recent recording studies have pointed to the retrosplenial cortex, along with the anatomically linked parietal cortex, as having a critical role in coding an animal’s position along a route: in particular, both regions contain neural populations that fire preferentially in locations along a fixed path, and in relation to specific movement actions that make up the route, for example left or right turns [7–9]. Secondly, retrosplenial neurons are modulated both by location within a route and by the location of the route in relation to the global environment [9]. This observation mirrors recent electrophysiological work showing that populations of retrosplenial head direction cells — neurons that fire when the animal’s head is in a specific direction — can be sensitive to local cues, while at the same time other populations of retrosplenial head direction cells are anchored to global cues [10]. Thirdly, lesions of retrosplenial cortex produce impairments in directional orientation based on landmarks [11]. These observations are further supported by human neuroimaging studies in which subjects navigate virtual environments: such studies have found that the retrosplenial cortex is strongly engaged when subjects utilize local geometric features or global cues to accurately orient [12,13]. In their study, Alexander and Nitz [3] recorded populations of retrosplenial neurons while rats navigated through a plus-shaped track requiring the animal to engage in several repeating action sequences along a fixed route. As previously reported [9], retrosplenial neurons tended to fire maximally at particular locations in the maze, indicating that cell activity encodes an animal’s position along the route. Interestingly, many retrosplenial neurons spiked in a repeating, periodic spatial pattern along the path. This spiking pattern tended to localize along route segments that involved a similar
sequence of movements. For instance, some cells would spike at segments that included a right turn followed by a left turn, while others would spike along segments occupying a left turn followed by a right turn. When navigating rats were restricted to navigate through a shortened portion of the track, retrosplenial cells tended to express the same periodic pattern for that segment of the track. The consistent pattern of activity across full-length and shortened tracks suggests that route segments may be mapped in relation to the distal or global environment. Alexander and Nitz [3] further report three important characteristics of periodic firing by retrosplenial cells. Firstly, different retrosplenial cells spiked at different spatial scales; in other words, some neurons exhibited elevated spatial firing along a broad segment of the path, while others spiked according to two or four repeating path segments. Secondly, it was observed that some cells simultaneously represented more than one spatial scale. This conjunctive coding was particularly apparent in cell populations that displayed elevated firing along a broad single segment of the path, while showing repeated spiking in one or more additional route segments. Finally, the authors determined that spiking by a subpopulation of broadly tuned cells was largely symmetrical for two halves of the route. Importantly, this latter finding suggests a neural mechanism by which the distance between route-segments might be encoded. It is well documented that retrosplenial neurons can be modulated by locomotor variables such as angular or linear velocity that tend to occur at sharp turns along complex routes [9,14]. Because the plus-track environment included several turn locations that repeat along the route, periodic activity by retrosplenial neurons could be due to a bias in the movements made at these symmetrical locations. Alexander and Nitz [3] first determined that, although a subset of retrosplenial cells were modulated by movement correlates, a majority were not. Next, they tested whether the periodic activity exhibited by retrosplenial neurons in the plus-track would generalize to a ring-shaped track. Importantly, unlike the plus-track, the ring-track lacked distinct route
R650 Current Biology 27, R642–R666, July 10, 2017
segments composed of sharp right and left turns; furthermore, locomotor variables such as angular and linear velocity were roughly held constant in each lap of the maze. As in the plustrack, the authors identified neural correlates that reflected a single location, two locations, and four locations. But they noted that neural modulation along four segments of the ring-track was diminished relative to the plus-track. This is perhaps not surprising given the absence of sharp turns on the ring-track, and given the fact that many cells exhibiting modulation in four segments of the plus-track were also significantly modulated by angular velocity. Nevertheless, the finding supports the general conclusion that retrosplenial activity reflects the spatial structure of the local environment, rather than simply mirroring movement speed. How are periodic signals generated in the retrosplenial cortex? This is not yet understood, but as Alexander and Nitz [3] note, it is likely relevant that the retrosplenial cortex is anatomically linked with parahippocampal cortical regions [4–6], which contain grid cells that spike in multiple locations forming a repeating hexagonal pattern in an environment [15]. Different grid cells fire in different locations and orientations, but also fire at different spatial scales (the size and distance between firing fields varies between cells). Also notable is the increase in spatial scale in the tuning width of head direction cells in layer III of the medial entorhinal cortex [16]. It will be important to determine whether variation in retrosplenial route coding might be influenced by external parahippocampal inputs, or whether the signal is generated by a separate neural system or a consequence of intrinsic circuitry. Based on this new evidence [3], an important future step will be to update theoretical and computational work with respect to the role of retrosplenial cortex in spatial navigation. For instance, a striking feature of navigation deficits after retrosplenial damage are the descriptions of patients reporting an inability to determine which way to go in relation to landmarks, termed topographic (or heading) disorientation [17]. While these deficits could be interpreted in relation to the loss of landmark use for directional
Current Biology
Dispatches orientation [11,13,18], or an inability in translating between viewer-centered (egocentric) and allocentric reference frames [19], the findings by Alexander and Nitz [3] point to a potential impairment in mapping the appropriate path structure to a goal location. In summary, the report by Alexander and Nitz [3] provides novel evidence that the retrosplenial cortex generates a unique signal that may reflect a mapping of route segments and the relationship between these segments. The findings raise questions regarding the emergence of periodic neural firing in retro-entorhinal circuitry and the consequences of this novel signal on spatial behavior and memory.
4. Harker, K.T., and Whishaw, I.Q. (2004). A reaffirmation of the retrosplenial contributions to rodent navigation: reviewing the influence of lesion, strain, and task. Neurosci. Biobehav. Rev. 28, 485–496.
12. Marchett, S.A., Vass, L.K., Ryan, J., and Epstein, R.A. (2014). Anchoring the neural compass: coding of local spatial reference frames in human medial parietal lobe. Nat. Neurosci. 17, 1598–1606.
5. Vann, S.D., Aggleton, J.P., and Maguire, E.A. (2009). What does the retrosplenial cortex do? Nat. Rev. Neurosci. 10, 792–802.
13. Shine, J.P., Valdes-Herrera, J.P., Hegerty, M., and Wolbers, T. (2016). The human retrosplenial cortex and thalamus code head direction in a global reference frame. J. Neurosci. 36, 6371–6381.
REFERENCES
9. Alexander, A.S., and Nitz, D.A. (2015). Retrosplenial cortex maps the conjunction of internal and external spaces. Nat. Neurosci. 18, 1143–1151.
1. O’Keefe, J., and Nadel, L. (1978). The Hippocampus as a Cognitive Map (Oxford, England: Oxford University Press). 2. Knierim, J.J., and Hamilton, D.A. (2011). Framing Spatial Cognition: Neural representations of proximal and distal frames of reference and their roles in navigation. Physiol. Rev. 91, 1245–1279. 3. Alexander, A.S., and Nitz, D.A. (2017). Spatially periodic activation patterns of retrosplenial cortex encode route sub-spaces and distance traveled. Curr. Biol. 27, 1551–1560.e4.
6. Bucci, D.J., and Robinson, S. (2014). Toward a conceptualization of retrohippocampal contributions to learning and memory. Neurobiol. Learn. Mem. 116, 197–207. 7. Nitz, D.A. (2006). Tracking route progression in the posterior parietal cortex. Neuron 49, 747–756. 8. Wilber, A.A., Clark, B.J., Forster, T.C., Tatsuno, M., and McNaughton, B.L. (2014). Interaction of egocentric and world-centered reference frames in the rat posterior parietal cortex. J. Neurosci. 34, 5431–5446.
10. Jacob, P.Y., Casali, G., Spieser, L., Page, H., Overington, D., and Jeffery, K. (2017). An independent, landmark-dominated headdirection signal in dysgranular retrosplenial cortex. Nat. Neurosci. 20, 173–175. 11. Clark, B.J., Bassett, J.P., Wang, S., and Taube, J.S. (2010). Impaired head direction cell representation in the anterodorsal thalamus after lesions of the retrosplenial cortex. J. Neurosci. 30, 5289–5302.
14. Cho, J., and Sharp, P.E. (2001). Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. Behav. Neurosci. 115, 3–25. 15. Moser, E.I., Kropff, E., and Moser, M.B. (2008). Place cells, grid cells, and the brain’s spatial representation system. Annu. Rev. Neurosci. 31, 69–89. 16. Giocomo, L.M., Stensola, T., Bonnevie, T., Van Cauter, T., Moser, M.B., and Moser, E.I. (2014). Topography of head direction cells in medial entorhinal cortex. Curr. Biol. 24, 252–262. 17. Aguirre, G.K., and D’Esposito, M. (1999). Topographical disorientation: a synthesis and taxonomy. Brain. 122, 1613–1628. 18. Bicanski, A., and Burgess, N. (2016). Environmental anchoring of head direction in a computational model of retrosplenial cortex. J. Neurosci. 36, 11601–11618. 19. Byrne, P., Becker, S., and Burgess, N. (2007). Remembering the past and imagining the future: a neural model of spatial memory and imagery. Psychol. Rev. 114, 340–375.
Evolution: King-Size Plastid Genomes in a New Red Algal Clade David Moreira* and Purificacio´n Lo´pez-Garcı´a
matique Evolution, CNRS, Universite Paris-Sud, AgroParisTech, Universite Paris-Saclay, 91400, Orsay, France Ecologie Syste *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2017.05.038
Plastids, the photosynthetic organelles of eukaryotes, exhibit remarkably stable genome architecture. However, a recent study of microscopic red algae has found new record-sized plastid genomes with unusual architectures. These species form a new branch in the tree of red algae. More than one billion years ago, a heterotrophic protist engulfed a cyanobacterium which, instead of being digested immediately, established a long-term symbiotic relationship with its predator. This cyanobacterium transformed into a stable cell organelle, the plastid, and allowed the birth of the
first photosynthetic eukaryotes. This evolutionary event had planetary consequences since photosynthetic eukaryotes occupied new ecological niches, diversified extraordinarily and became major players in the global carbon cycle. Three eukaryotic phyla are the direct descendants of this
cyanobacterial endosymbiosis: the rare and poorly-known glaucophyte algae and the much more widespread and species-rich red algae, green algae and land plants [1]. Both red and green algae have been privileged targets of study for several generations of biologists and their
Current Biology 27, R642–R666, July 10, 2017 ª 2017 Elsevier Ltd. R651
Dispatches 2. Fry, B.G., Roelants, K., Champagne, D.E., Scheib, H., Tyndall, J.D.A., King, G.F., Nevalainen, T.J., Norman, J.A., Lewis, R.J., Norton, R.S., et al. (2009). The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu. Rev. Genomics. Hum. Genet. 10, 483–511. 3. Chang, D., and Duda, T.F. (2012). Extensive and continuous duplication facilitates rapid evolution and diversification of gene families. Mol. Biol. Evol. 29, 2019–2029.
patterns of platypus defensin and related venom genes across a range of tissue types reveal the possibility of broader functions for OvDLPs than previously suspected. Toxicon 52, 559–565. 9. Hargreaves, A.D., Swain, M.T., Hegarty, M.J., Logan, D.W., and Mulley, J.F. (2014). Restriction and recruitment-gene duplication and the origin and evolution of snake venom toxins. Genome Biol. Evol. 6, 2088– 2095.
4. Vonk, F.J., Casewell, N.R., Henkel, C.V., Heimberg, A.M., Jansen, H.J., McCleary, R.J.R., Kerkkamp, H.M., Vos, R.A., Guerreiro, I., Calvete, J.J., et al. (2013). The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. Proc. Natl. Acad. Sci. USA 110, 20651–20656.
10. Junqueira-de-Azevedo, I.L.M., Bastos, C.M.V., Ho, P.L., Luna, M.S., Yamanouye, N., and Casewell, N.R. (2015). Venom-related transcripts from Bothrops jararaca tissues provide novel molecular insights into the production and evolution of snake venom. Mol. Biol. Evol. 32, 754–766.
5. Sanggaard, K.W., Bechsgaard, J.S., Fang, X., Duan, J., Dyrlund, T.F., Gupta, V., Jiang, X., Cheng, L., Fan, D., Feng, Y., et al. (2014). Spider genomes provide insight into composition and evolution of venom and silk. Nat. Commun. 5, 3765.
11. Reyes-Velasco, J., Card, D.C., Andrew, A.L., Shaney, K.J., Adams, R.H., Schield, D.R., Casewell, N.R., Mackessy, S.P., and Castoe, T.A. (2015). Expression of venom gene homologs in diverse python tissues suggests a new model for the evolution of snake venom. Mol. Biol. Evol. 32, 173–183.
6. Martinson, E., Mrinalini, Kelkar, Y.D., Chang, C.-H., and Werren, J.H. (2017). The evolution of venom by co-option of single copy genes. Curr. Biol. 27, 2007–2013. 7. Wang, X., Gao, B., and Zhu, S. (2016). Exon shuffling and origin of scorpion venom biodiversity. Toxins (Basel) 9, 10.
12. Margres, M.J., Bigelow, A.T., Lemmon, E.M., Lemmon, A.R., and Rokyta, D.R. (2017). Selection to increase expression, not sequence diversity, precedes gene family origin and expansion in rattlesnake venom. Genetics. http://dx.doi.org/10.1534/genetics. 117.202655.
8. Whittington, C.M., Papenfuss, A.T., Kuchel, P.W., and Belov, K. (2008). Expression
13. Nei, M., Gu, X., and Sitnikova, T. (1997). Evolution by the birth-and-death process in
multigene families of the vertebrate immune system. Proc. Natl. Acad. Sci. USA 94, 7799– 7806. 14. Sunagar, K., Moran, Y., Salemi, M., Chen, L., Wang, Y., and Pond, S.K. (2015). The rise and fall of an evolutionary innovation: contrasting strategies of venom evolution in ancient and young animals. PLOS Genet. 11, e1005596. 15. Terlau, H., and Olivera, B.M. (2004). Conus venoms: a rich source of novel ion channeltargeted peptides. Physiol. Rev. 84, 41–68. 16. Martinson, E.O., Wheeler, D., Wright, J., Mrinalini, Siebert, A.L., and Werren, J.H. (2014). Nasonia vitripennis venom causes targeted gene expression changes in its fly host. Mol. Ecol. 23, 5918–5930. 17. Mrinalini, Siebert, A.L., Wright, J., Martinson, E., Wheeler, D., and Werren, J.H. (2015). Parasitoid venom induces metabolic cascades in fly hosts. Metabolomics 11, 350–366. 18. Wong, E.S.W., Papenfuss, A.T., Whittington, C.M., Warren, W.C., and Belov, K. (2012). A limited role for gene duplications in the evolution of platypus venom. Mol. Biol. Evol. 29, 167–177. 19. Conant, G.C., and Wolfe, K.H. (2008). Turning a hobby into a job: how duplicated genes find new functions. Nat. Rev. Genet. 9, 938–950. 20. Smith, C.W., and Valca´rcel, J. (2000). Alternative pre-mRNA splicing: the logic of combinatorial control. Trends Biochem. Sci. 25, 381–388.
Spatial Navigation: Retrosplenial Cortex Encodes the Spatial Structure of Complex Routes Benjamin J. Clark Department of Psychology, University of New Mexico, MSC03 2220, 1 University of New Mexico, Albuquerque, NM 87131, USA Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2017.05.019
A new study in which recordings were made from the retrosplenial cortex while rats navigated through a complex environment has revealed populations of cells that encode route-segments as well as the relative position of these segments within an allocentric framework. There is considerable evidence that animals, including humans, can navigate by referencing the geometric contours and cues defining a local environment, while at the same time monitoring their position and direction in relation to a global or allocentric framework [1,2]. The capacity to make use of both local and global frames of reference allows for ease in navigation in which subjects may
rapidly alter their sequence of movements, or their route, towards a goal. These can involve a large-scale modification in the structure of the route, or a mere update to a small segment of the path. Flexible changes in route structure suggest that animals may retain information regarding the action patterns that make up a route, while at
the same time keeping track of the relationships between the various routesegments. The mechanisms by which route structure is processed at local and global spatial scales are poorly understood, but work published recently in Current Biology by Alexander and Nitz [3] suggests a role for neurons in the retrosplenial cortex, a dorsal cortical structure that occupies a pivotal
Current Biology 27, R642–R666, July 10, 2017 ª 2017 Elsevier Ltd. R649
Current Biology
Dispatches position between posterior sensory and limbic-hippocampal systems, and that has been linked to integrative functions such as spatial navigation and memory [4–6]. A number of previous observations have indicated that retrosplenial cortex may be involved in route planning. Firstly, recent recording studies have pointed to the retrosplenial cortex, along with the anatomically linked parietal cortex, as having a critical role in coding an animal’s position along a route: in particular, both regions contain neural populations that fire preferentially in locations along a fixed path, and in relation to specific movement actions that make up the route, for example left or right turns [7–9]. Secondly, retrosplenial neurons are modulated both by location within a route and by the location of the route in relation to the global environment [9]. This observation mirrors recent electrophysiological work showing that populations of retrosplenial head direction cells — neurons that fire when the animal’s head is in a specific direction — can be sensitive to local cues, while at the same time other populations of retrosplenial head direction cells are anchored to global cues [10]. Thirdly, lesions of retrosplenial cortex produce impairments in directional orientation based on landmarks [11]. These observations are further supported by human neuroimaging studies in which subjects navigate virtual environments: such studies have found that the retrosplenial cortex is strongly engaged when subjects utilize local geometric features or global cues to accurately orient [12,13]. In their study, Alexander and Nitz [3] recorded populations of retrosplenial neurons while rats navigated through a plus-shaped track requiring the animal to engage in several repeating action sequences along a fixed route. As previously reported [9], retrosplenial neurons tended to fire maximally at particular locations in the maze, indicating that cell activity encodes an animal’s position along the route. Interestingly, many retrosplenial neurons spiked in a repeating, periodic spatial pattern along the path. This spiking pattern tended to localize along route segments that involved a similar
sequence of movements. For instance, some cells would spike at segments that included a right turn followed by a left turn, while others would spike along segments occupying a left turn followed by a right turn. When navigating rats were restricted to navigate through a shortened portion of the track, retrosplenial cells tended to express the same periodic pattern for that segment of the track. The consistent pattern of activity across full-length and shortened tracks suggests that route segments may be mapped in relation to the distal or global environment. Alexander and Nitz [3] further report three important characteristics of periodic firing by retrosplenial cells. Firstly, different retrosplenial cells spiked at different spatial scales; in other words, some neurons exhibited elevated spatial firing along a broad segment of the path, while others spiked according to two or four repeating path segments. Secondly, it was observed that some cells simultaneously represented more than one spatial scale. This conjunctive coding was particularly apparent in cell populations that displayed elevated firing along a broad single segment of the path, while showing repeated spiking in one or more additional route segments. Finally, the authors determined that spiking by a subpopulation of broadly tuned cells was largely symmetrical for two halves of the route. Importantly, this latter finding suggests a neural mechanism by which the distance between route-segments might be encoded. It is well documented that retrosplenial neurons can be modulated by locomotor variables such as angular or linear velocity that tend to occur at sharp turns along complex routes [9,14]. Because the plus-track environment included several turn locations that repeat along the route, periodic activity by retrosplenial neurons could be due to a bias in the movements made at these symmetrical locations. Alexander and Nitz [3] first determined that, although a subset of retrosplenial cells were modulated by movement correlates, a majority were not. Next, they tested whether the periodic activity exhibited by retrosplenial neurons in the plus-track would generalize to a ring-shaped track. Importantly, unlike the plus-track, the ring-track lacked distinct route
R650 Current Biology 27, R642–R666, July 10, 2017
segments composed of sharp right and left turns; furthermore, locomotor variables such as angular and linear velocity were roughly held constant in each lap of the maze. As in the plustrack, the authors identified neural correlates that reflected a single location, two locations, and four locations. But they noted that neural modulation along four segments of the ring-track was diminished relative to the plus-track. This is perhaps not surprising given the absence of sharp turns on the ring-track, and given the fact that many cells exhibiting modulation in four segments of the plus-track were also significantly modulated by angular velocity. Nevertheless, the finding supports the general conclusion that retrosplenial activity reflects the spatial structure of the local environment, rather than simply mirroring movement speed. How are periodic signals generated in the retrosplenial cortex? This is not yet understood, but as Alexander and Nitz [3] note, it is likely relevant that the retrosplenial cortex is anatomically linked with parahippocampal cortical regions [4–6], which contain grid cells that spike in multiple locations forming a repeating hexagonal pattern in an environment [15]. Different grid cells fire in different locations and orientations, but also fire at different spatial scales (the size and distance between firing fields varies between cells). Also notable is the increase in spatial scale in the tuning width of head direction cells in layer III of the medial entorhinal cortex [16]. It will be important to determine whether variation in retrosplenial route coding might be influenced by external parahippocampal inputs, or whether the signal is generated by a separate neural system or a consequence of intrinsic circuitry. Based on this new evidence [3], an important future step will be to update theoretical and computational work with respect to the role of retrosplenial cortex in spatial navigation. For instance, a striking feature of navigation deficits after retrosplenial damage are the descriptions of patients reporting an inability to determine which way to go in relation to landmarks, termed topographic (or heading) disorientation [17]. While these deficits could be interpreted in relation to the loss of landmark use for directional
Current Biology
Dispatches orientation [11,13,18], or an inability in translating between viewer-centered (egocentric) and allocentric reference frames [19], the findings by Alexander and Nitz [3] point to a potential impairment in mapping the appropriate path structure to a goal location. In summary, the report by Alexander and Nitz [3] provides novel evidence that the retrosplenial cortex generates a unique signal that may reflect a mapping of route segments and the relationship between these segments. The findings raise questions regarding the emergence of periodic neural firing in retro-entorhinal circuitry and the consequences of this novel signal on spatial behavior and memory.
4. Harker, K.T., and Whishaw, I.Q. (2004). A reaffirmation of the retrosplenial contributions to rodent navigation: reviewing the influence of lesion, strain, and task. Neurosci. Biobehav. Rev. 28, 485–496.
12. Marchett, S.A., Vass, L.K., Ryan, J., and Epstein, R.A. (2014). Anchoring the neural compass: coding of local spatial reference frames in human medial parietal lobe. Nat. Neurosci. 17, 1598–1606.
5. Vann, S.D., Aggleton, J.P., and Maguire, E.A. (2009). What does the retrosplenial cortex do? Nat. Rev. Neurosci. 10, 792–802.
13. Shine, J.P., Valdes-Herrera, J.P., Hegerty, M., and Wolbers, T. (2016). The human retrosplenial cortex and thalamus code head direction in a global reference frame. J. Neurosci. 36, 6371–6381.
REFERENCES
9. Alexander, A.S., and Nitz, D.A. (2015). Retrosplenial cortex maps the conjunction of internal and external spaces. Nat. Neurosci. 18, 1143–1151.
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Evolution: King-Size Plastid Genomes in a New Red Algal Clade David Moreira* and Purificacio´n Lo´pez-Garcı´a
matique Evolution, CNRS, Universite Paris-Sud, AgroParisTech, Universite Paris-Saclay, 91400, Orsay, France Ecologie Syste *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2017.05.038
Plastids, the photosynthetic organelles of eukaryotes, exhibit remarkably stable genome architecture. However, a recent study of microscopic red algae has found new record-sized plastid genomes with unusual architectures. These species form a new branch in the tree of red algae. More than one billion years ago, a heterotrophic protist engulfed a cyanobacterium which, instead of being digested immediately, established a long-term symbiotic relationship with its predator. This cyanobacterium transformed into a stable cell organelle, the plastid, and allowed the birth of the
first photosynthetic eukaryotes. This evolutionary event had planetary consequences since photosynthetic eukaryotes occupied new ecological niches, diversified extraordinarily and became major players in the global carbon cycle. Three eukaryotic phyla are the direct descendants of this
cyanobacterial endosymbiosis: the rare and poorly-known glaucophyte algae and the much more widespread and species-rich red algae, green algae and land plants [1]. Both red and green algae have been privileged targets of study for several generations of biologists and their
Current Biology 27, R642–R666, July 10, 2017 ª 2017 Elsevier Ltd. R651