Skip to main content Accessibility help
×
Hostname: page-component-848d4c4894-tn8tq Total loading time: 0 Render date: 2024-06-20T13:30:11.207Z Has data issue: false hasContentIssue false

Chapter 6 - Lamprey Thalamus and Beyond

from Section 3: - Evolution

Published online by Cambridge University Press:  12 August 2022

Michael M. Halassa
Affiliation:
Massachusetts Institute of Technology
Get access

Summary

The lampreys (Cyclostomes) represent the oldest group of now-living vertebrates that diverged from the vertebrate evolutionary line leading to mammals 560 million years ago. It is therefore of particular interest to consider if there is a thalamus similar to that of other vertebrates and examine how it is organised. The lamprey thalamus relays both visual and somatosensory information to the cortex (also called the pallium). In addition, the thalamus receives input from both the optic tectum (superior colliculus) and pretectum, as in other vertebrates, and there is, furthermore, a thalamic projection to the striatum from cells located in the periventricular area of the thalamus. Essentially, the basic compartments of the mammalian thalamus are thus represented in the lamprey but with a much smaller number of neurons. The implication is that the essential features of the thalamus had already evolved at the point when the cyclostome lineage diverged from that leading to other vertebrates. We review here what is known regarding the lamprey thalamus from the perspective of anatomy, transmitters, and neurophysiology and also how it compares to mammals, as well as other groups of vertebrates.

Type
Chapter
Information
The Thalamus , pp. 125 - 138
Publisher: Cambridge University Press
Print publication year: 2022

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Benito-Gutiérrez, È., Stemmer, M., Rohr, S.D., Schuhmacher, L.N., Tang, J., Marconi, A., Jékely, G., and Arendt, D. (2018). Patterning of a telencephalon-like region in the adult brain of amphioxus. bioRxiv, 307629.Google Scholar
Bloch, S., Hagio, H., Thomas, M., Heuze, A., Hermel, J.M., Lasserre, E., Colin, I., Saka, K., Affaticati, P., Jenett, A., et al. (2020). Non-thalamic origin of zebrafish sensory nuclei implies convergent evolution of visual pathways in amniotes and teleosts. eLife 9, e54945.Google Scholar
Bourassa, J., and Deschênes, M. (1995). Corticothalamic projections from the primary visual cortex in rats: a single fiber study using biocytin as an anterograde tracer. Neuroscience 66, 253263.Google Scholar
Braasch, I., Gehrke, A.R., Smith, J.J., Kawasaki, K., Manousaki, T., Pasquier, J., Amores, A., Desvignes, T., Batzel, P., Catchen, J., et al. (2016). The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons. Nat Genet 48, 427437.CrossRefGoogle ScholarPubMed
Braford, M.R.J., and Northcutt, R.G. (1983). Organization of the diencephalon and pretectum of the ray-finned fishes. In Neurobiology, Vol 2: Higher Brain Areas and Functions, Davis, R.E., and Northcutt, R.G., eds. (Ann Arbor: University of Michigan Press), pp. 117164.Google Scholar
Briscoe, S.D., and Ragsdale, C.W. (2019). Evolution of the chordate telencephalon. Curr Biol 29, R647R662.CrossRefGoogle ScholarPubMed
Butler, A.B. (1994). The evolution of the dorsal thalamus of jawed vertebrates, including mammals: cladistic analysis and a new hypothesis. Brain Res Brain Res Rev 19, 2965.CrossRefGoogle Scholar
Butler, A.B. (1995). The dorsal thalamus of jawed vertebrates: a comparative viewpoint. Brain Behav Evol 46, 209223.Google Scholar
Butler, A.B. (2008). Evolution of brains, cognition, and consciousness. Brain Res Bull 75, 442449.Google Scholar
Butler, A.B., and Hodos, W. (2005). Comparative Vertebrate Neuroanatomy: Evolution and Adaptation, 2nd edn (New Jersey: Wiley).Google Scholar
Butler, A.B., and Saidel, W.M. (1993). Retinal projections in teleost fishes: Patterns, variations, and questions. Comp Biochem Physiol Part A 104, 431442.Google Scholar
Capantini, L., von Twickel, A., Robertson, B., and Grillner, S. (2017). The pretectal connectome in lamprey. J Comp Neurol 525, 753772.CrossRefGoogle ScholarPubMed
Cleland, B.G., Dubin, M.W., and Levick, W.R. (1971). Simultaneous recording of input and output of lateral geniculate neurones. Nat New Biol 231, 191192.Google Scholar
Cohen, D.H., Duff, T.A., and Ebbesson, S.O. (1973). Electrophysiological identification of a visual area in shark telencephalon. Science 182, 492494.Google Scholar
Comoli, E., Das Neves Favaro, P., Vautrelle, N., Leriche, M., Overton, P.G., and Redgrave, P. (2012). Segregated anatomical input to sub-regions of the rodent superior colliculus associated with approach and defense. Front Neuroanat 6, 9.Google Scholar
Crabtree, J.W. (2018). Functional diversity of thalamic reticular subnetworks. Front Syst Neurosci 12, 41.Google Scholar
Deschênes, M., Bourassa, J., and Pinault, D. (1994). Corticothalamic projections from layer V cells in rat are collaterals of long-range corticofugal axons. Brain Res 664, 215219.Google Scholar
Drager, U.C. (1975). Receptive fields of single cells and topography in mouse visual cortex. J Comp Neurol 160, 269290.CrossRefGoogle ScholarPubMed
Dubuc, R., Bongianni, F., Ohta, Y., and Grillner, S. (1993a). Anatomical and physiological study of brainstem nuclei relaying dorsal column inputs in lampreys. J Comp Neurol 327, 260270.Google Scholar
Dubuc, R., Bongianni, F., Ohta, Y., and Grillner, S. (1993b). Dorsal root and dorsal column mediated synaptic inputs to reticulospinal neurons in lampreys: involvement of glutamatergic, glycinergic, and GABAergic transmission. J Comp Neurol 327, 251259.Google Scholar
Dugas-Ford, J., and Ragsdale, C.W. (2015). Levels of homology and the problem of neocortex. Annu Rev Neurosci 38, 351368.Google Scholar
Ebbesson, S.O., and Hodde, K.C. (1981). Ascending spinal systems in the nurse shark, Ginglymostoma cirratum. Cell Tissue Res 216, 313331.CrossRefGoogle ScholarPubMed
Ebbesson, S.O., and Schroeder, D.M. (1971). Connections of the nurse shark’s telencephalon. Science 173, 254256.Google Scholar
Echteler, S.M., and Saidel, W.M. (1981). Forebrain connections in the goldfish support telencephalic homologies with land vertebrates. Science 212, 683685.Google Scholar
Erisir, A., Van Horn, S.C., and Sherman, S.M. (1997). Relative numbers of cortical and brainstem inputs to the lateral geniculate nucleus. Proc Natl Acad Sci USA 94, 15171520.Google Scholar
Feinberg, T.E., and Mallatt, J. (2017). Corrigendum to “The Nature of Primary Consciousness. A New Synthesis” [Conscious Cogn. 43 (2016) 113–127]. Conscious Cogn 48, 293.Google Scholar
Fournier, J., Muller, C.M., Schneider, I., and Laurent, G. (2018). Spatial information in a non-retinotopic visual cortex. Neuron 97, 164–180 e167.CrossRefGoogle Scholar
González, A., Lopez, J.M., Morona, R., and Moreno, N. (2020). The organization of the central nervous system of amphibians. In Evolutionary Neuroscience, Kaas, J.H., ed. (Oxford: Academic Press), pp. 125157.Google Scholar
Grillner, S., and Robertson, B. (2016). The basal ganglia over 500 million years. Curr Biol 26, R1088R1100.Google Scholar
Grillner, S., Robertson, B., and Kotaleski Hellgren, J. (2020). Basal ganglia—a motion perspective. Compr Physiol 10, 12411275.Google Scholar
Guillery, R. (2017). The Brain as a Tool. A Neuroscientist’s Account (Oxford: Oxford University Press).Google Scholar
Hall, J.A., Foster, R.E., Ebner, F.F., and Hall, W.C. (1977). Visual cortex in a reptile, the turtle (Pseudemys scripta and Chrysemys picta). Brain Res 130, 197216.Google Scholar
Heap, L.A.L., Vanwalleghem, G., Thompson, A.W., Favre-Bulle, I.A., and Scott, E.K. (2018). Luminance changes drive directional startle through a thalamic pathway. Neuron 99, 293–301 e294.Google Scholar
Heier, P. (1948). Fundamental properties in the structure of the brain. A study of the brain of Petromyzon marinus. Acta Anat 8, 3213.Google Scholar
Heimberg, A.M., Cowper-Sal-lari, R., Semon, M., Donoghue, P.C., and Peterson, K.J. (2010). microRNAs reveal the interrelationships of hagfish, lampreys, and gnathostomes and the nature of the ancestral vertebrate. Proc Natl Acad Sci USA 107, 1937919383.Google Scholar
Helmbrecht, T.O., Dal Maschio, M., Donovan, J.C., Koutsouli, S., and Baier, H. (2018). Topography of a visuomotor transformation. Neuron 100, 1429–1445 e1424.Google Scholar
Herrick, C.J. (1948). The Brain of the Tiger Salamander, Ambystoma tigrinum (Chicago: University of Chicago Press).Google Scholar
Ishikawa, Y., Yamamoto, N., Yoshimoto, M., Yasuda, T., Maruyama, K., Kage, T., Takeda, H., and Ito, H. (2007). Developmental origin of diencephalic sensory relay nuclei in teleosts. Brain Behav Evol 69, 8795.Google Scholar
Ito, T., and Atoji, Y. (2016). Tectothalamic inhibitory projection neurons in the avian torus semicircularis. J Comp Neurol 524, 26042622.Google Scholar
Jones, M.R., Grillner, S., and Robertson, B. (2009). Selective projection patterns from subtypes of retinal ganglion cells to tectum and pretectum: distribution and relation to behavior. J Comp Neurol 517, 257275.Google Scholar
Kaas, J.H. (2004). Somatosensory system. In The Human Nervous System, Paxinos, G., and Mai, J.K., eds. (New York: Elsevier), pp. 10591092.Google Scholar
Kaas, J.H., Nelson, R.J., Sur, M., Lin, C.S., and Merzenich, M.M. (1979). Multiple representations of the body within the primary somatosensory cortex of primates. Science 204, 521523.Google Scholar
Karten, H.J. (2015). Vertebrate brains and evolutionary connectomics: on the origins of the mammalian “neocortex.” Philos Trans R Soc Lond B Biol Sci 370.Google Scholar
Kenigfest, N.B., and Belekhova, M.G. (2009). [Evolutionary significance of reciprocal connections in the turtle tectofugal visual system]. Zh Evol Biokhim Fiziol 45, 334342.Google Scholar
Krubitzer, L.A., and Kaas, J.H. (1992). The somatosensory thalamus of monkeys: cortical connections and a redefinition of nuclei in marmosets. J Comp Neurol 319, 123140.Google Scholar
Kumar, S., and Hedges, S.B. (1998). A molecular timescale for vertebrate evolution. Nature 392, 917920.Google Scholar
Kunst, M., Laurell, E., Mokayes, N., Kramer, A., Kubo, F., Fernandes, A.M., Forster, D., Dal Maschio, M., and Baier, H. (2019). A Cellular-resolution atlas of the larval zebrafish brain. Neuron 103, 21–38 e25.Google Scholar
Lamanna, F, Hervas-Sotomayor F, A.P. O, Jandzik D, Sobrido-Cameán D, Martik ML, Green SA, Brüning T, Mößinger K, Schmidt J, et al.: Reconstructing the ancestral vertebrate brain using a lamprey neural cell type atlas. BioRxiv 2022.Google Scholar
Luiten, P.G. (1981a). Two visual pathways to the telencephalon in the nurse shark (Ginglymostoma cirratum). I. Retinal projections. J Comp Neurol 196, 531538.Google Scholar
Luiten, P.G. (1981b). Two visual pathways to the telencephalon in the nurse shark (Ginglymostoma cirratum). II. Ascending thalamo-telencephalic connections. J Comp Neurol 196, 539548.Google Scholar
Ma, M., Kler, S., and Pan, Y.A. (2019). Structural neural connectivity analysis in zebrafish with restricted anterograde transneuronal viral labeling and quantitative brain mapping. Front Neural Circuits 13, 85.Google Scholar
Marin, O., Gonzalez, A., and Smeets, W.J. (1997a). Basal ganglia organization in amphibians: afferent connections to the striatum and the nucleus accumbens. J Comp Neurol 378, 1649.Google Scholar
Marin, O., Gonzalez, A., and Smeets, W.J. (1997b). Basal ganglia organization in amphibians: efferent connections of the striatum and the nucleus accumbens. J Comp Neurol 380, 2350.Google Scholar
Matesz, C., and Szekely, G. (1978). The motor column and sensory projections of the branchial cranial nerves in the frog. J Comp Neurol 178, 157176.Google Scholar
Medina, L., and Reiner, A. (2000). Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends Neurosci 23, 112.Google Scholar
Medina, M., Reperant, J., Ward, R., Rio, J.P., and Lemire, M. (1993). The primary visual system of flatfish: an evolutionary perspective. Anat Embryol (Berl) 187, 167191.CrossRefGoogle ScholarPubMed
Miyashita, T., Coates, M.I., Farrar, R., Larson, P., Manning, P.L., Wogelius, R.A., Edwards, N.P., Anne, J., Bergmann, U., Palmer, A.R., et al. (2019). Hagfish from the Cretaceous Tethys Sea and a reconciliation of the morphological-molecular conflict in early vertebrate phylogeny. Proc Natl Acad Sci USA 116, 21462151.Google Scholar
Morona, R., and Gonzalez, A. (2008). Calbindin-D28k and calretinin expression in the forebrain of anuran and urodele amphibians: further support for newly identified subdivisions. J Comp Neurol 511, 187220.Google Scholar
Morona, R., Lopez, J.M., and Gonzalez, A. (2011). Localization of calbindin-d28k and calretinin in the brain of Dermophis mexicanus (amphibia: gymnophiona) and its bearing on the interpretation of newly recognized neuroanatomical regions. Brain Behav Evol 77, 231269.Google Scholar
Mueller, T. (2012). What is the thalamus in zebrafish? Front Neurosci 6, 64.Google Scholar
Mundell, N.A., Beier, K.T., Pan, Y.A., Lapan, S.W., Goz Ayturk, D., Berezovskii, V.K., Wark, A.R., Drokhlyansky, E., Bielecki, J., Born, R.T., et al. (2015). Vesicular stomatitis virus enables gene transfer and transsynaptic tracing in a wide range of organisms. J Comp Neurol 523, 16391663.Google Scholar
Munoz, A., Munoz, M., Gonzalez, A., and Ten Donkelaar, H.J. (1995). Anuran dorsal column nucleus: organization, immunohistochemical characterization, and fiber connections in Rana perezi and Xenopus laevis. J Comp Neurol 363, 197220.Google Scholar
Nieuwenhuys, R., and Nicholson, C. (1998). Lampreys (Petromyzontoidea). In The Central Nervous System of Vertebrates, Nieuwenhuys, R., Donkelaar, H.J.T., and Nicholson, C., eds. (Berlin, Heidelberg: Springer), pp. 397495.Google Scholar
Nieuwenhuys, R., ten Donkelaar, H.J., and Nicholson, C. (1998). The Central Nervous System of Vertebrates (Berlin, Heidelberg: Springer).Google Scholar
Northcutt, R.G., and Butler, A.B. (1976). Retinofugal pathways in the lingnose gar Lepisosteus osseus (linnaeus). J Comp Neurol 166, 115.Google Scholar
Northcutt, R.G., and Butler, A.B. (1980). Projections of the optic tectum in the longnose gar, Lepisosteus osseus. Brain Res 190, 333346.Google Scholar
Northcutt, R.G., and Kicliter, E. (1980). Organization of the amphibian telencephalon. In Comparative Neurology of the Telencephalon, Ebbesson, S.O.E., ed. (Boston, MA: Springer).Google Scholar
Northcutt, R.G., and Wicht, H. (1997). Afferent and efferent connections of the lateral and medial pallia of the silver lamprey. Brain Behav Evol 49, 119.Google Scholar
Ocana, F.M., Suryanarayana, S.M., Saitoh, K., Kardamakis, A.A., Capantini, L., Robertson, B., and Grillner, S. (2015). The lamprey pallium provides a blueprint of the mammalian motor projections from cortex. Curr Biol 25, 413423.Google Scholar
Parichy, D.M. (2016). The gar is a fish… is a bird… is a mammal? Nat Genet 48, 344345.CrossRefGoogle Scholar
Patel, M.B., Sons, S., Yudintsev, G., Lesicko, A.M., Yang, L., Taha, G.A., Pierce, S.M., and Llano, D.A. (2017). Anatomical characterization of subcortical descending projections to the inferior colliculus in mouse. J Comp Neurol 525, 885900.Google Scholar
Perez-Fernandez, J., Kardamakis, A.A., Suzuki, D.G., Robertson, B., and Grillner, S. (2017). Direct dopaminergic projections from the SNc modulate visuomotor transformation in the lamprey tectum. Neuron 96, 910–924 e915.Google Scholar
Perez-Fernandez, J., Stephenson-Jones, M., Suryanarayana, S.M., Robertson, B., and Grillner, S. (2014). Evolutionarily conserved organization of the dopaminergic system in lamprey: SNc/VTA afferent and efferent connectivity and D2 receptor expression. J Comp Neurol 522, 37753794.Google Scholar
Pombal, M.A., and Puelles, L. (1999). Prosomeric map of the lamprey forebrain based on calretinin immunocytochemistry, Nissl stain, and ancillary markers. J Comp Neurol 414, 391422.Google Scholar
Puelles, L. (2017). Comments on the updated tetrapartite pallium model in the mouse and chick, featuring a homologous claustro-insular complex. Brain Behav Evol 90, 171189.Google Scholar
Ravi, V., and Venkatesh, B. (2018). The divergent genomes of teleosts. Annu Rev Anim Biosci 6, 4768.Google Scholar
Reiner, A. (1993). Neurotransmitter organization and connections of turtle cortex: implications for the evolution of mammalian isocortex. Comp Biochem Physiol Comp Physiol 104, 735748.Google Scholar
Reiner, A., Yamamoto, K., and Karten, H.J. (2005). Organization and evolution of the avian forebrain. Anat Rec A Discov Mol Cell Evol Biol 287, 10801102.CrossRefGoogle ScholarPubMed
Roth, G., Blanke, J., and Ohle, M. (1995). Brain size and morphology in miniaturized plethodontid salamanders. Brain Behav Evol 45, 8495.Google Scholar
Roth, G., Nishikawa, K.C., Naujoks-Manteuffel, C., Schmidt, A., and Wake, D.B. (1993). Paedomorphosis and simplification in the nervous system of salamanders. Brain Behav Evol 42, 137170.Google Scholar
Schneider, G.E. (1969). Two visual systems. Science 163, 895902.Google Scholar
Sincich, L.C., Zhang, Y., Tiruveedhula, P., Horton, J.C., and Roorda, A. (2009). Resolving single cone inputs to visual receptive fields. Nat Neurosci 12, 967969.Google Scholar
Smeets, W.J. (1982). The afferent connections of the tectum mesencephali in two chondrichthyans, the shark Scyliorhinus canicula and the ray Raja clavata. J Comp Neurol 205, 139152.Google Scholar
Smeets, W.J. (1992). Comparative aspects of basal forebrain organization in vertebrates. Eur J Morphol 30, 2336.Google Scholar
Stephenson-Jones, M., Ericsson, J., Robertson, B., and Grillner, S. (2012). Evolution of the basal ganglia: dual-output pathways conserved throughout vertebrate phylogeny. J Comp Neurol 520, 29572973.Google Scholar
Stephenson-Jones, M., Samuelsson, E., Ericsson, J., Robertson, B., and Grillner, S. (2011). Evolutionary conservation of the basal ganglia as a common vertebrate mechanism for action selection. Curr Biol 21, 10811091.Google Scholar
Striedter, G.F. (1990a). The diencephalon of the channel catfish, Ictalurus punctatus. I. Nuclear organization. Brain Behav Evol 36, 329354.CrossRefGoogle ScholarPubMed
Striedter, G.F. (1990b). The diencephalon of the channel catfish, Ictalurus punctatus. II. Retinal, tectal, cerebellar and telencephalic connections. Brain Behav Evol 36, 355377.Google Scholar
Sugahara, F., Murakami, Y., Pascual-Anaya, J., and Kuratani, S. (2017). Reconstructing the ancestral vertebrate brain. Dev Growth Differ 59, 163174.Google Scholar
Sugahara, F., Pascual-Anaya, J., Oisi, Y., Kuraku, S., Aota, S., Adachi, N., Takagi, W., Hirai, T., Sato, N., Murakami, Y., et al. (2016). Evidence from cyclostomes for complex regionalization of the ancestral vertebrate brain. Nature 531, 97100.Google Scholar
Suryanarayana, S.M., Perez-Fernandez, J., Robertson, B., and Grillner, S. (2020). The evolutionary origin of visual and somatosensory representation in the vertebrate pallium. Nat Ecol Evol 4, 639651.Google Scholar
Suryanarayana, S.M., Pérez-Fernández, J., Robertson, B., and Grillner, S. (2021). Olfaction in lamprey pallium revisited—dual projections of mitral and tufted cells. Cell Reports 34.Google Scholar
Suryanarayana, S.M., Robertson, B., Wallen, P., and Grillner, S. (2017). The lamprey pallium provides a blueprint of the mammalian layered cortex. Curr Biol 27, 3264–3277 e3265.Google Scholar
ten Donkelaar, H.J. (1998). Urodeles. In The Central Nervous System of Vertebrates, Nieuwenhuys, R., ten Donkelaar, H.J., and Nicolson, C., eds. (Berlin, Heidelberg: Springer), pp. 10451150.Google Scholar
Ulinski, P.S. (1986). Organization of corticogeniculate projections in the turtle, Pseudemys scripta. J Comp Neurol 254, 529542.CrossRefGoogle ScholarPubMed
Villar-Cervino, V., Barreiro-Iglesias, A., Mazan, S., Rodicio, M.C., and Anadon, R. (2011). Glutamatergic neuronal populations in the forebrain of the sea lamprey, Petromyzon marinus: an in situ hybridization and immunocytochemical study. J Comp Neurol 519, 17121735.Google Scholar
Westhoff, G., and Roth, G. (2002). Morphology and projection pattern of medial and dorsal pallial neurons in the frog Discoglossus pictus and the salamander Plethodon jordani. J Comp Neurol 445, 97121.Google Scholar
Westhoff, G., Roth, G., and Straka, H. (2004). Topographic representation of vestibular and somatosensory signals in the anuran thalamus. Neuroscience 124, 669683.Google Scholar
Wicht, H., and Himstedt, W. (1988). Topologic and connectional analysis of the dorsal thalamus of Triturus alpestris (amphibia, urodela, salamandridae). J Comp Neurol 267, 545561.Google Scholar
Wild, J.M. (1997). The avian somatosensory system: the pathway from wing to Wulst in a passerine (Chloris chloris). Brain Res 759, 122134.Google Scholar
Wullimann, M.F., and Mueller, T. (2004). Teleostean and mammalian forebrains contrasted: Evidence from genes to behavior. J Comp Neurol 475, 143162.Google Scholar
Wullimann, M.F., and Northcutt, R.G. (1990). Visual and electrosensory circuits of the diencephalon in mormyrids: an evolutionary perspective. J Comp Neurol 297, 537552.Google Scholar
Yamamoto, N., and Ito, H. (2008). Visual, lateral line, and auditory ascending pathways to the dorsal telencephalic area through the rostrolateral region of the lateral preglomerular nucleus in cyprinids. J Comp Neurol 508, 615647.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×