Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The evolutionary origin of visual and somatosensory representation in the vertebrate pallium

Nature Ecology & Evolution volume 4, pages 639–651 (2020)Cite this article

Subjects

Abstract

Amniotes, such as mammals and reptiles, have vision and other senses represented in the pallium, whereas anamniotes, such as amphibians, fish and cyclostomes (including lampreys), which diverged much earlier, were historically thought to process olfactory information predominantly or even exclusively in the pallium. Here, we show that there is a separate visual area with retinotopic representation, and that somatosensory information from the head and trunk is represented in an adjacent area in the lamprey pallial cortex (lateral pallium). These cortical sensory areas flank a non-primary-sensory motor area. Both vision and somatosensation are relayed via the thalamus. These findings suggest that the basic sensorimotor representation of the mammalian neocortex, as well as the sensory thalamocortical relay, had already evolved in the last common ancestor of cyclostomes and gnathostomes around 560 million years ago.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: A visual region in the dorsal part of the lateral pallium responds to retinal stimulation with retinotopy.
Fig. 2: Characterizing visual pallial neurons.
Fig. 3: Somatosensory region in the dorsal part of the lateral pallium.
Fig. 4: Projections from the DCN to the thalamus.
Fig. 5: Thalamic relay to the visual area.
Fig. 6: Visual, somatosensory and motor organization in the lamprey cortex and phylogenetic vertebrate tree.

Data availability

All data generated or analysed during this study are included within the published article and its Supplementary Information files.

References

  1. Kumar, S. & Hedges, S. B. A molecular timescale for vertebrate evolution. Nature 392, 917–920 (1998).

    Article  CAS  PubMed  Google Scholar 

  2. Suzuki, D. G. & Grillner, S. The stepwise development of the lamprey visual system and its evolutionary implications. Biol. Rev. Camb. Phil. Soc. 93, 1461–1477 (2018).

    Article  Google Scholar 

  3. Suzuki, D. G., Perez-Fernandez, J., Wibble, T., Kardamakis, A. A. & Grillner, S. The role of the optic tectum for visually evoked orienting and evasive movements. Proc. Natl Acad. Sci. USA 116, 15272–15281 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Woolsey, C. N. in Biological and Biochemical Bases of Behaviour (eds Harlow, H. F. & Woolsey, C. N.) 63–81 (Univ. Wisconsin Press, 1958).

  5. Dugas-Ford, J. & Ragsdale, C. W. Levels of homology and the problem of neocortex. Annu. Rev. Neurosci. 38, 351–368 (2015).

    Article  CAS  PubMed  Google Scholar 

  6. Briscoe, S. D. & Ragsdale, C. W. Evolution of the chordate telencephalon. Curr. Biol. 29, R647–R662 (2019).

    Article  CAS  PubMed  Google Scholar 

  7. Kaas, J. H. The evolution of brains from early mammals to humans. Wiley Interdiscip. Rev. Cogn. Sci. 4, 33–45 (2013).

    Article  PubMed  Google Scholar 

  8. Harting, J. K., Huerta, M. F., Hashikawa, T. & van Lieshout, D. P. Projection of the mammalian superior colliculus upon the dorsal lateral geniculate nucleus: organization of tectogeniculate pathways in nineteen species. J. Comp. Neurol. 304, 275–306 (1991).

    Article  CAS  PubMed  Google Scholar 

  9. Tohmi, M., Meguro, R., Tsukano, H., Hishida, R. & Shibuki, K. The extrageniculate visual pathway generates distinct response properties in the higher visual areas of mice. Curr. Biol. 24, 587–597 (2014).

    Article  CAS  PubMed  Google Scholar 

  10. Berkley, K. J. Spatial relationships between the terminations of somatic sensory and motor pathways in the rostral brainstem of cats and monkeys. I. Ascending somatic sensory inputs to lateral diencephalon. J. Comp. Neurol. 193, 283–317 (1980).

    Article  CAS  PubMed  Google Scholar 

  11. Casas-Torremocha, D., Clasca, F. & Nunez, A. Posterior thalamic nucleus modulation of tactile stimuli processing in rat motor and primary somatosensory cortices. Front. Neural Circuits 11, 69 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Guido, W. Development, form, and function of the mouse visual thalamus. J. Neurophysiol. 120, 211–225 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Fournier, J., Muller, C. M., Schneider, I. & Laurent, G. Spatiali in a non-retinotopic visual cortex. Neuron 97, 164–180.e7 (2018).

    Article  CAS  PubMed  Google Scholar 

  14. Laurent, G. et al. in Micro-, Meso- and Macro-Dynamics of the Brain (eds Buzsaki, G. & Christen, Y.) 23–33 (Springer International Publishing, 2016).

  15. Butler, A. B. The evolution of the dorsal pallium in the telencephalon of amniotes: cladistic analysis and a new hypothesis. Brain Res. Rev. 19, 66–101 (1994).

    Article  CAS  PubMed  Google Scholar 

  16. Karten, H. J. The organization of the avian telencephalon and some speculations on the phylogeny of the amniote telencephalon. Ann. NY Acad. Sci. 167, 164–179 (1969).

    Article  Google Scholar 

  17. Karten, H. J. Neocortical evolution: neuronal circuits arise independently of lamination. Curr. Biol. 23, R12–R15 (2013).

    Article  CAS  PubMed  Google Scholar 

  18. Krubitzer, L. The magnificent compromise: cortical field evolution in mammals. Neuron 56, 201–208 (2007).

    Article  CAS  PubMed  Google Scholar 

  19. Medina, L. & Reiner, A. Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends Neurosci. 23, 1–12 (2000).

    Article  CAS  PubMed  Google Scholar 

  20. Wild, J. M. The avian somatosensory system: the pathway from wing to Wulst in a passerine (Chloris chloris). Brain Res. 759, 122–134 (1997).

    Article  CAS  PubMed  Google Scholar 

  21. Wild, J. M. in Sturkie’s Avian Physiology (ed. Scanes, C. G.) 55–69 (Academic Press, 2015).

  22. Defelipe, J. The evolution of the brain, the human nature of cortical circuits, and intellectual creativity. Front. Neuroanat. 5, 29 (2011).

    PubMed  PubMed Central  Google Scholar 

  23. Karamian, A. I., Vesselkin, N. P., Belekhova, M. G. & Zagorulko, T. M. Electrophysiological characteristics of tectal and thalamo-cortical divisions of the visual system in lower vertebrates. J. Comp. Neurol. 127, 559–576 (1966).

    Article  CAS  PubMed  Google Scholar 

  24. Northcutt, R. G. & Wicht, H. Afferent and efferent connections of the lateral and medial pallia of the silver lamprey. Brain Behav. Evol. 49, 1–19 (1997).

    Article  CAS  PubMed  Google Scholar 

  25. Wicht, H. & Northcutt, R. G. Telencephalic connections in the Pacific hagfish (Eptatretus stouti), with special reference to the thalamopallial system. J. Comp. Neurol. 395, 245–260 (1998).

    Article  CAS  PubMed  Google Scholar 

  26. Suryanarayana, S. M., Robertson, B., Wallen, P. & Grillner, S. The lamprey pallium provides a blueprint of the mammalian layered cortex. Curr. Biol. 27, 3264–3277.e5 (2017).

    Article  CAS  PubMed  Google Scholar 

  27. Ocana, F. M. et al. The lamprey pallium provides a blueprint of the mammalian motor projections from cortex. Curr. Biol. 25, 413–423 (2015).

    Article  CAS  PubMed  Google Scholar 

  28. Northcutt, R. G. & Ronan, M. Afferent and efferent connections of the bullfrog medial pallium. Brain Behav. Evol. 40, 1–16 (1992).

    Article  CAS  PubMed  Google Scholar 

  29. Cohen, D. H., Duff, T. A. & Ebbesson, S. O. Electrophysiological identification of a visual area in shark telencephalon. Science 182, 492–494 (1973).

    Article  CAS  PubMed  Google Scholar 

  30. Ishikawa, Y. et al. Developmental origin of diencephalic sensory relay nuclei in teleosts. Brain Behav. Evol. 69, 87–95 (2007).

    Article  PubMed  Google Scholar 

  31. Ito, H., Murakami, T., Fukuoka, T. & Kishida, R. Thalamic fiber connections in a teleost (Sebastiscus marmoratus): visual somatosensory, octavolateral, and cerebellar relay region to the telencephalon. J. Comp. Neurol. 250, 215–227 (1986).

    Article  CAS  PubMed  Google Scholar 

  32. Vernier, P. in Evolution of Nervous Systems Vol. 1 (ed. Kaas, J. H.) 59–75 (Academic Press, 2017).

  33. Yamamoto, N. et al. A new interpretation on the homology of the teleostean telencephalon based on hodology and a new eversion model. Brain Behav. Evol. 69, 96–104 (2007).

    Article  PubMed  Google Scholar 

  34. Yamamoto, N. & Ito, H. Fiber connections of the anterior preglomerular nucleus in cyprinids with notes on telencephalic connections of the preglomerular complex. J. Comp. Neurol. 491, 212–233 (2005).

    Article  PubMed  Google Scholar 

  35. Kardamakis, A. A., Saitoh, K. & Grillner, S. Tectal microcircuit generating visual selection commands on gaze-controlling neurons. Proc. Natl Acad. Sci. USA 112, E1956–E1965 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Perez-Fernandez, J., Kardamakis, A. A., Suzuki, D. G., Robertson, B. & Grillner, S. Direct dopaminergic projections from the SNc modulate visuomotor transformation in the lamprey tectum. Neuron 96, 910–924.e5 (2017).

    Article  CAS  PubMed  Google Scholar 

  37. Dubuc, R., Bongianni, F., Ohta, Y. & Grillner, S. Anatomical and physiological study of brainstem nuclei relaying dorsal column inputs in lampreys. J. Comp. Neurol. 327, 260–270 (1993).

    Article  CAS  PubMed  Google Scholar 

  38. Nieuwenhuys, R. & Nicholson, C. in The Central Nervous System of Vertebrates Vol. 1 (eds Nieuwenhuys, R., ten Donkelaar, H. J. & Nicholson, C.) 397–495 (Springer, 1997).

  39. De Miguel, E., Rodicio, M. C. & Anadon, R. Organization of the visual system in larval lampreys: an HRP study. J. Comp. Neurol. 302, 529–542 (1990).

    Article  CAS  PubMed  Google Scholar 

  40. Heier, P. Fundamental principles in the structure of the brain. A study of the brain of Petromyzon fluviatilis. Acta Anat. Suppl. 6, 1–213 (1948).

    Article  Google Scholar 

  41. Kennedy, M. C. & Rubinson, K. Retinal projections in larval, transforming and adult sea lamprey, Petromyzon marinus. J. Comp. Neurol. 171, 465–479 (1977).

    Article  CAS  PubMed  Google Scholar 

  42. Robertson, B., Auclair, F., Menard, A., Grillner, S. & Dubuc, R. GABA distribution in lamprey is phylogenetically conserved. J. Comp. Neurol. 503, 47–63 (2007).

    Article  CAS  PubMed  Google Scholar 

  43. Jones, M. R., Grillner, S. & Robertson, B. Selective projection patterns from subtypes of retinal ganglion cells to tectum and pretectum: distribution and relation to behavior. J. Comp. Neurol. 517, 257–275 (2009).

    Article  PubMed  Google Scholar 

  44. Douglas, R. J. & Martin, K. A. Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 27, 419–451 (2004).

    Article  CAS  PubMed  Google Scholar 

  45. Ferster, D., Chung, S. & Wheat, H. Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 380, 249–252 (1996).

    Article  CAS  PubMed  Google Scholar 

  46. Goulas, A., Majka, P., Rosa, M. G. P. & Hilgetag, C. C. A blueprint of mammalian cortical connectomes. PLoS Biol. 17, e2005346 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Markram, H. et al. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5, 793–807 (2004).

    Article  CAS  PubMed  Google Scholar 

  48. Harris, K. D. & Shepherd, G. M. The neocortical circuit: themes and variations. Nat. Neurosci. 18, 170–181 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Shepherd, G. M. The microcircuit concept applied to cortical evolution: from three-layer to six-layer cortex. Front. Neuroanat. 5, 30 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  50. Briscoe, S. D. & Ragsdale, C. W. Homology, neocortex, and the evolution of developmental mechanisms. Science 362, 190–193 (2018).

    Article  CAS  PubMed  Google Scholar 

  51. Karten, H. J. Vertebrate brains and evolutionary connectomics: on the origins of the mammalian ‘neocortex’. Phil. Trans. R Soc. Lond. B Biol. Sci. 370, 20150060 (2015).

    Article  Google Scholar 

  52. Klingler, E. Development and organization of the evolutionarily conserved three-layered olfactory cortex. eNeuro 4, e0193-16.2016 (2017).

    Article  Google Scholar 

  53. Fournier, J., Muller, C. M. & Laurent, G. Looking for the roots of cortical sensory computation in three-layered cortices. Curr. Opin. Neurobiol. 31, 119–126 (2015).

    Article  CAS  PubMed  Google Scholar 

  54. Tosches, M. A. et al. Evolution of pallium, hippocampus, and cortical cell types revealed by single-cell transcriptomics in reptiles. Science 360, 881–888 (2018).

    Article  CAS  PubMed  Google Scholar 

  55. Raghanti, M. A. et al. in Evolution of Nervous Systems 2e Vol. 4 (ed. Kaas, J. H.) 267–289 (Elsevier, 2017).

  56. Brodmann, K. Brodmann’s: Localisation in the Cerebral Cortex (Springer, 2006).

  57. Krubitzer, L. A. & Prescott, T. J. The combinatorial creature: cortical phenotypes within and across lifetimes. Trends Neurosci. 41, 744–762 (2018).

    Article  CAS  PubMed  Google Scholar 

  58. Pombal, M. A., Megias, M., Bardet, S. M. & Puelles, L. New and old thoughts on the segmental organization of the forebrain in lampreys. Brain Behav. Evol. 74, 7–19 (2009).

    Article  PubMed  Google Scholar 

  59. Puelles, L. Comments on the updated tetrapartite pallium model in the mouse and chick, featuring a homologous claustro-insular complex. Brain Behav. Evol. 90, 171–189 (2017).

    Article  PubMed  Google Scholar 

  60. Puelles, L., Alonso, A., Garcia-Calero, E. & Martinez-de-la-Torre, M. Concentric ring topology of mammalian cortical sectors and relevance for patterning studies. J. Comp. Neurol. 527, 1731–1752 (2019).

    Article  PubMed  Google Scholar 

  61. Montiel, J. F. & Aboitiz, F. Homology in amniote brain evolution: the rise of molecular evidence. Brain Behav. Evol. 91, 59–64 (2018).

    Article  PubMed  Google Scholar 

  62. Tosches, M. A. & Laurent, G. Evolution of neuronal identity in the cerebral cortex. Curr. Opin. Neurobiol. 56, 199–208 (2019).

    Article  CAS  PubMed  Google Scholar 

  63. Dugas-Ford, J., Rowell, J. J. & Ragsdale, C. W. Cell-type homologies and the origins of the neocortex. Proc. Natl Acad. Sci. USA 109, 16974–16979 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  64. Huang, Z. J. & Paul, A. The diversity of GABAergic neurons and neural communication elements. Nat. Rev. Neurosci. 20, 563–572 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Sugahara, F. et al. Evidence from cyclostomes for complex regionalization of the ancestral vertebrate brain. Nature 531, 97–100 (2016).

    Article  CAS  PubMed  Google Scholar 

  66. Bayramov, A. V. et al. The presence of Anf/Hesx1 homeobox gene in lampreys suggests that it could play an important role in emergence of telencephalon. Sci. Rep. 6, 39849 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Martinez-de-la-Torre, M., Pombal, M. A. & Puelles, L. Distal-less-like protein distribution in the larval lamprey forebrain. Neuroscience 178, 270–284 (2011).

    Article  CAS  PubMed  Google Scholar 

  68. Sugahara, F., Murakami, Y., Pascual-Anaya, J. & Kuratani, S. Reconstructing the ancestral vertebrate brain. Dev. Growth Differ. 59, 163–174 (2017).

    Article  PubMed  Google Scholar 

  69. Noro, M., Sugahara, F. & Kuraku, S. Reevaluating Emx gene phylogeny: homopolymeric amino acid tracts as a potential factor obscuring orthology signals in cyclostome genes. BMC Evol. Biol. 15, 78 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Carrera, I., Ferreiro-Galve, S., Sueiro, C., Anadon, R. & Rodriguez-Moldes, I. Tangentially migrating GABAergic cells of subpallial origin invade massively the pallium in developing sharks. Brain Res. Bull. 75, 405–409 (2008).

    Article  CAS  PubMed  Google Scholar 

  71. Garcia-Moreno, F. et al. Absence of tangentially migrating glutamatergic neurons in the developing avian brain. Cell Rep. 22, 96–109 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Murakami, Y. et al. Identification and expression of the lamprey Pax6 gene: evolutionary origin of the segmented brain of vertebrates. Development 128, 3521–3531 (2001).

    CAS  PubMed  Google Scholar 

  73. Puelles, L. Thoughts on the development, structure and evolution of the mammalian and avian telencephalic pallium. Phil. Trans. R Soc. Lond. B Biol. Sci. 356, 1583–1598 (2001).

    Article  CAS  Google Scholar 

  74. Grillner, S. & Robertson, B. The basal ganglia over 500 million years. Curr. Biol. 26, R1088–R1100 (2016).

    Article  CAS  PubMed  Google Scholar 

  75. Perez-Fernandez, J., Stephenson-Jones, M., Suryanarayana, S. M., Robertson, B. & Grillner, S. Evolutionarily conserved organization of the dopaminergic system in lamprey: SNc/VTA afferent and efferent connectivity and D2 receptor expression. J. Comp. Neurol. 522, 3775–3794 (2014).

    Article  CAS  PubMed  Google Scholar 

  76. Stephenson-Jones, M., Floros, O., Robertson, B. & Grillner, S. Evolutionary conservation of the habenular nuclei and their circuitry controlling the dopamine and 5-hydroxytryptophan (5-HT) systems. Proc. Natl Acad. Sci. USA 109, E164–E173 (2012).

    Article  PubMed  Google Scholar 

  77. Stephenson-Jones, M., Kardamakis, A. A., Robertson, B. & Grillner, S. Independent circuits in the basal ganglia for the evaluation and selection of actions. Proc. Natl Acad. Sci. USA 110, E3670–E3679 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  78. Stephenson-Jones, M., Samuelsson, E., Ericsson, J., Robertson, B. & Grillner, S. Evolutionary conservation of the basal ganglia as a common vertebrate mechanism for action selection. Curr. Biol. 21, 1081–1091 (2011).

    Article  CAS  PubMed  Google Scholar 

  79. Institute of Laboratory Animal Research NRC Guide for the Care and Use of Laboratory Animals (National Academy Press, 1996).

Download references

Acknowledgements

We thank A. El Manira, G. Silberberg and P. Wallén for valuable comments on the manuscript. We are indebted to P. Löw for the anti-synaptotagmin antibody. This work was supported by the Swedish Medical Research Council (VR-M-K2013-62X-03026, VR-M-2015-02816 and VR-M-2018-02453), the European Union Seventh Framework Programme (FP7/2007-2013) under grant agreement number 604102 (Human Brain Project), EU/Horizon 2020 numbers 720270 (HBP SGA1) and 785907 (HBP SGA2), Parkinsonfonden and the Karolinska Institutet’s research funds.

Author information

Authors and Affiliations

  1. Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden

    Shreyas M. Suryanarayana, Juan Pérez-Fernández, Brita Robertson & Sten Grillner

Authors
  1. Shreyas M. Suryanarayana
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan Pérez-Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Brita Robertson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sten Grillner
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S.M.S. and S.G. conceived of the study. S.M.S., J.P.-F., B.R. and S.G. designed the experiments. S.M.S. and J.P.-F. performed the experiments. All authors participated in data analysis and discussion of the results. S.G. and S.M.S. wrote the manuscript with input from B.R. and J.P.-F. S.G. supervised all aspects of the study and sourced the funding.

Corresponding author

Correspondence to Sten Grillner.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Local gabazine injection in visual cortex leads to loss of retinotopy, related to Fig. 1.

a, Schematic showing the recording site in the visual cortex and local injection of gabazine. b, Schematic of the retina showing locations of different stimulation sites (colour coded) c, During control conditions, for the recording site shown in a (orange) there is an ON response (blue trace) for one stimulation site in the retina, whereas for the other sites there is an OFF response (black traces). Following local injection of gabazine in the visual area, the same recording site shows a long-lasting and sustained activity (red traces) for all four stimulation sites in the retina, showing a loss of retinotopic specificity. LPal, lateral pallium.

Extended Data Fig. 2 Visual cortical neurons, related to Fig. 1.

a, Photomicrograph of lateral pallium/cortex showing the location of visual cortical neurons labelled intracellularly with Neurobiotin (magenta) during recordings. b, Confocal image of a spiny (arrowheads) dendrite of a visual pallial cell. c, Photomicrograph showing the location of anterogradely labelled thalamic afferents in the medial pallium. The visual cortical neurons send some of their dendrites into the medial pallium (see Fig. 2) where they receive thalamic input. d, Transverse schematic sections of the pallium showing the distribution and location of the visual cortical neurons. dmtn, dorsomedial telencephalic nucleus; LPal, lateral pallium; MPal, medial pallium; nII, optic nerve; Str, striatum.

Extended Data Fig. 3 Relay of trigeminal input to thalamus, related to Fig. 3.

a, Schematic showing the location of the trigeminal sensory nucleus (dotted square) and the injection site in contralateral thalamus (blue) to retrogradely label neurons in the trigeminal sensory nucleus referred to also as the nucleus of the radix descendens nervi trigemini. b, Photomicrograph showing retrogradely labelled neurons in the trigeminal sensory nucleus projecting to thalamus. c, Transverse schematics showing the location of retrogradely labelled neurons projecting to the contralateral thalamus (blue dots) in the trigeminal sensory nucleus, as well as the descending root of the trigeminal nerve (magenta). d, Confocal photomicrograph showing a retrogradely labelled cell of the trigeminal sensory nucleus projecting to thalamus (blue) sending its dendrite into the trigeminal tract (magenta) where it receives synapses (green) from the descending root of the trigeminal nerve f. Box diagram showing the trigeminal sensory pathway from the trigeminal sensory nerve to the somatosensory cortex. drV, descending root of the trigeminal nerve; IX, glossopharyngeal motor nucleus; X, vagus motor nucleus; PRRN, posterior rhombencephalon reticular nucleus.

Extended Data Fig. 4 Thalamocortical neurons also send collaterals to the optic tectum retinotopically, related to Fig. 5.

a, Retrogradely double-labelled cells (arrowheads) in the dorsolateral thalamus following Neurobiotin injection in the lateral pallium (green) and dextran-rhodamine in the tectum (magenta), showing that these thalamocortical cells also send a collateral to tectum. b, Dual injections of dextran-Alexa 647 (green) and dextran-rhodamine (magenta) in the rostral and caudal tectum, respectively, showing distinct non-overlapping labelled neuronal subpopulations in the dorsolateral thalamus (arrowheads), indicating that these thalamic neurons are specific in their projections to the tectal retinotopic map. c, Distinct population of neurons retrogradely labelled in the periventricular area of the dorsal thalamus following dextran-Alexa 647 (red, arrow) and dextran-rhodamine (magenta, arrowhead) in the rostral and caudal tectum, respectively. Both neuronal subpopulations are additionally retrogradely labelled following Neurobiotin injections (green) in pallium, indicating that these periventricular thalamic neurons, that target tectum with retinotopic specificity, also project to pallium. d, Summarising schematic of the thalamus showing two subpopulations retrogradely labelled from rostral (green) and caudal (magenta) tectum in both the lateral and periventricular regions, some of which also project to pallium (outer blue ring). Hb, habenula; LPal, lateral pallium; ot, optic tract; Th, thalamus.

Extended Data Fig. 5 Retinotopic specificity at three levels of visual processing in the lamprey brain, related to Figs. 1 and 5.

Schematic drawings of the lateral pallium, thalamus and optic tectum showing that the retinotopically organised afferents from the retina target specific subgroups of thalamic neurons, which project to both visual pallium and tectum. This highlights the overall maintenance of retinotopic specificity at the three different levels of visual processing in the lamprey brain—visual pallium, thalamus and optic tectum. Hb, habenula; LPal, lateral pallium; ot, optic tract; Th, thalamus.

Extended Data Fig. 6 Thalamic projections to different sensory areas of pallium, as well as the projections to striatum are distinct, related to Figs. 1, 3 and 5.

a, Photomicrographs of the thalamus showing distinct subpopulations of neurons retrogradely labelled following dextran-rhodamine (magenta, arrows) and dextran-Alexa 647 (yellow, arrowhead) in the pallial visual and somatosensory areas, respectively, as well as Neurobiotin injection (green, arrow) in the striatum. b, Photomicrograph showing the different injection sites. LPal, lateral pallium; Str, striatum. c, Schematic of pallium and transverse sections of thalamus and striatum showing that distinct subgroups of thalamic neurons target different sensory areas in pallium and striatum. Hb, habenula; Hyp, hypothalamus; LPal, lateral pallium; MPal, medial pallium; nII, optic nerve; ot, optic tract; Th, thalamus.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Suryanarayana, S.M., Pérez-Fernández, J., Robertson, B. et al. The evolutionary origin of visual and somatosensory representation in the vertebrate pallium. Nat Ecol Evol 4, 639–651 (2020). https://doi.org/10.1038/s41559-020-1137-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-020-1137-2

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing