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The Lamprey Pallium Provides a Blueprint of the Mammalian Motor Projections from Cortex

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The Lamprey Pallium Provides a Blueprint of the Mammalian Motor Projections from Cortex Article The Lamprey Pallium Provides a Blueprint of the Mammalian Motor Projections from Cortex Graphical Abstract Authors Francisco M. Ocan˜ a, Shreyas M. Suryanarayana, ..., Brita Robertson, Sten Grillner Correspondence [email protected] In Brief Ocan˜ a et al. show that the mammalian organization with a motor cortex from which different classes of movements can be elicited was present already at the dawn of vertebrate evolution, 560 million years ago, when the lamprey line of evolution diverged from that leading to mammals. Detailed connectivity and synaptic properties are also conserved. Highlights d Pallial/cortical motor projections evolved at the dawn of vertebrate evolution d Stimulation of pallial areas in lamprey elicits eye, trunk, or oral movements d Pallial projection neurons target midbrain, reticulospinal areas, and basal ganglia d Pallial stimulation evokes monosynaptic EPSPs in tectal and reticulospinal neurons Ocan˜ a et al., 2015, Current Biology 25, 413–423 February 16, 2015 ª2015 Elsevier Ltd All rights reserved http://dx.doi.org/10.1016/j.cub.2014.12.013 Current Biology 25, 413–423, February 16, 2015 ª2015 Elsevier Ltd All rights reserved http://dx.doi.org/10.1016/j.cub.2014.12.013 Article The Lamprey Pallium Provides a Blueprint of the Mammalian Motor Projections from Cortex Francisco M. Ocan˜ a,1,2,3 Shreyas M. Suryanarayana,1,3 and habenulae, have recently been shown to be conserved Kazuya Saitoh,1 Andreas A. Kardamakis,1 in great detail [9–12]. Lorenza Capantini,1 Brita Robertson,1,4 and Sten Grillner1,4,* In addition to mammals, birds (corvids) are also considered 1The Nobel Institute for Neurophysiology, Department of to have an advanced cognitive ability [13]. Nevertheless, the Neuroscience, Karolinska Institutet, 171 77 Stockholm, bird pallium consists mainly of nuclear masses except for a Sweden small laminar structure, the wulst [14, 15]. Part of the avian 2Laboratory of Psychobiology, University of Sevilla, Campus forebrain can be regarded as comparable to the mammalian Santiago Ramo´ n y Cajal, 41018 Sevilla, Spain prefrontal cortex (see [16, 17]). Furthermore, layer-specific molecular markers for layer 4 and 5 cell types in mammals also stain cells in the pallium of birds and reptiles, suggesting Summary a common reptilian origin [18]. There is limited information concerning the pallium of fish, but efferent projections to the Background: The frontal lobe control of movement in mam- optic tectum and the mesencephalic tegmentum have been re- mals has been thought to be a specific function primarily ported [19, 20]. related to the layered neocortex with its efferent connections. In the present study, we examine whether the pallium in lam- In contrast, we now show that the same basic organization is prey is the evolutionary ‘‘ancestor’’ of the mammalian cortex present even in one of the phylogenetically oldest vertebrates, that directly controls the motor output repertoire. Stimulation the lamprey. of defined pallial sites elicits specific motor patterns including Results: Stimulation of specific sites in the pallium/cortex eye and orientation of the body mediated by glutamatergic evokes eye, trunk, locomotor, or oral movements. The pallial projections to downstream motor centers. Another core projection neurons target brainstem motor centers and basal aspect is the cortical/pallial control of the basal ganglia, via ganglia subnuclei and have prominent dendrites extending projections to the striatum and subthalamic nucleus. This in- into the outer molecular layer. They exhibit the characteristic cludes the two types of input from cortex/pallium—the collat- features of pyramidal neurons and elicit monosynaptic gluta- erals of the brainstem projecting neurons and the intratelence- matergic excitatory postsynaptic potentials in output neurons phalic projections (e.g., [21]). Thus, in contrast to what has of the optic tectum, reticulospinal neurons, and, as shown been assumed, the basic projection pattern of the vertebrate earlier, basal ganglia neurons. motor pallium/cortex had already evolved in the most ancient Conclusions: Our results demonstrate marked similarities in group of vertebrates, the lamprey, 560 million years ago [6], the efferent functional connectivity and control of motor and has been maintained throughout vertebrate evolution. behavior between the lamprey pallium and mammalian neocortex. Thus, the lamprey motor pallium/cortex represents Results an evolutionary blueprint of the corresponding mammalian system. Identification of a Pallial Motor Area from which Eye, Orienting, Locomotor, and Mouth Movements Can Be Elicited Introduction The pallium is the forebrain structure in lamprey, which corre- sponds to the cerebral cortex in mammals, in particular its The mammalian frontal lobe contains areas from which move- lateral part (LPal; see Figure 1A). We have explored the possi- ments of the eyes and different parts of the body can be eli- bility of whether movements could be elicited from this struc- cited [1–3]. These motor areas project to basal ganglia subnu- ture by microstimulation of its different parts at the dorsal sur- clei as well as to different centers in the midbrain, brainstem, face and at different depths (n = 22; Figure 1; Figure S1). We and spinal cord that coordinate the movements (e.g., [4, 5]). were able to show that stimulation of partially overlapping The layered neocortex of the frontal lobes has been thought areas in preferentially the middle to caudal part of the LPal to convey unique properties regarding the control of move- could elicit eye, orienting, swimming, or mouth movements ment and to be specific to mammals and different from that (Figure 1). The areas from which movements were elicited of other classes of vertebrates. Mammals and cyclostomes are indicated in Figures 1B–1E, with the lowest threshold in (lamprey) represent two extreme groups phylogenetically. By red (10–40 mA). Either one type of movement in isolation or a exploring the pallial (cortical) organization in one of the oldest combination of movements was produced, for instance eye groups of vertebrates [6], we show that the lamprey pallium/ and orienting movements and sometimes swimming or mouth cortex had already evolved a similar organization with respect movements. The depth distribution of low threshold activation to movement control early in vertebrate evolution. The role of is represented in Figures S1F–S1H, and the movements were the lamprey pallium has been practically unknown, except evoked mainly in the deeper parts of LPal often close to the for the projections to the striatum and their synaptic properties ventricle, where many of the projection neurons to the brain- [7–10]. Other forebrain structures, such as the basal ganglia stem are located (see Figure 5 below). Recordings of eye movements were performed with coils 3Co-first author mounted around the eye to detect the movements electromag- 4Co-senior author netically (Figures 2A and 2B; also see the Supplemental Exper- *Correspondence: [email protected] imental Procedures). Figure 2C shows that the eye movement 414 Figure 1. Threshold Maps for Different Types of ABC Movements (A) Dorsal schematic view of a lamprey brain showing the reconstructed distribution of electri- cally evoked motor responses. Data from 22 ani- mals were superimposed. (B–E) Color-coded contour plots representing the threshold current needed to evoke different motor patterns. Note that the excitability of the LPal decreases from the caudal to the rostral pole. DE The scale bars represent 500 mm. Hb, habenula; LPal, lateral pallium; MPal, medial pallium; OB, ol- factory bulb; OT, optic tectum; Pi, pineal gland; Rh, rhombencephalon. See also Figure S1. labeled fibers/terminals were present in pretectum, tectum, midbrain teg- mentum, and brainstem regions that in mammals receive direct descending amplitude increases with graded stimulation between 20 and projections from the motor cortex. These projections are 60 mA (pulse train of 30 Hz). With increasing stimulus intensity described in detail below. the latency decreases whereas the amplitude increases (Fig- Palliotectal Projections Are Glutamatergic and ures 2D–2F). Similarly, an increased stimulation frequency Monosynaptic from 10 to 60 Hz (Figures 2G–2J) will lead to a larger amplitude In the pretectum, a large bundle of efferent fibers (Neurobiotin movement (from 10 to 30 Hz) and a decrease of the latency. in red in Figure 3B) was observed on the dorsal aspect forming Finally, 95% of the evoked movements were contraversive to the palliopretectal/tectal pathway, with a few of these fibers the stimulated LPal (ipsilateral eye forward and contralateral crossing to the contralateral side. Arborizations were formed eye backward). This movement can be defined as an orienting around many of the cells in the dorsal pretectum (Figure 3B). movement, and changing stimulation parameters did not alter Further caudally in the optic tectum, efferent pallial fibers the direction of eye movements. entered dorsomedially to form terminal arborizations in the The orienting movements of the body were recorded with a deep motor output layer (Figure 3C), where tectal cells that video camera, and the angle between the fixed head and the project to the different brainstem regions are located (A.A. Kar- neck area was measured (Figures 2K and 2L; Figure S2). The damakis et al., 2013, Soc. Neurosci., abstract). The direct pro- amplitude of the movements increased with an increase in jection from the lamprey pallial region to tectum is comparable stimulation intensity from 25 up to 50 mA in a linear fashion (Fig- to the projections from the mammalian frontal eye field and the ure 2L). Such a movement would normally result in an orienting avian pallial gaze center to the collicular and tectal deep layers, movement of the head. If it instead would occur during respectively [22, 23]. swimming, it would lead to a turning movement in the same di- To examine the synaptic input from the motor pallium to the rection. Swimming movements were elicited less often (Fig- deep layer of tectum, whole-cell patch-clamp recordings were ure 1D), as were movements of the mouth (Figure 1E).
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