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

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.

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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.

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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.

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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.

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Correspondence to Sten Grillner.

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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.

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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

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