The dopaminergic system influences motor behavior, signals reward and novelty, and is an essential component of the basal ganglia in all vertebrates including the lamprey, one of the phylogenetically oldest vertebrates. The intrinsic organization and function of the lamprey basal ganglia is highly conserved. For instance, the direct and indirect pathways are modulated through dopamine D1 and D2 receptors in lamprey and in mammals. The nucleus of the tuberculum posterior, a homologue of the substantia nigra pars compacta (SNc)/ventral tegmental area (VTA) is present in lamprey, but only scarce data exist about its connectivity. Likewise, the D2 receptor is expressed in the striatum, but little is known about its localization in other brain areas. We used in situ hybridization and tracer injections, both in combination with tyrosine hydroxylase immunohistochemistry, to characterize the SNc/VTA efferent and afferent connectivity, and to relate its projection pattern with D2 receptor expression in particular. We show that most features of the dopaminergic system are highly conserved. As in mammals, the direct pallial (cortex in mammals) input and the basal ganglia connectivity with the SNc/VTA are present as part of the evaluation system, as well as input from the tectum as the evolutionary basis for salience/novelty detection. Moreover, the SNc/VTA receives sensory information from the olfactory bulbs, optic tectum, octavolateral area, and dorsal column nucleus, and it innervates, apart from the nigrostriatal pathway, several motor-related areas. This suggests that the dopaminergic system also contributes to the control of different motor centers at the brainstem level.
Amniotes, such as mammals and reptiles have vision and other senses represented in pallium, whereas anamniotes like amphibians, fish and cyclostomes (including lamprey) that diverged much earlier, were historically thought to process predominantly or even exclusively olfactory information in pallium. Here, we show here 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.The lamprey represents the oldest group of extant vertebrates 1 . It is an eel-like creature with a well-developed vision that lives a predatory parasitic life 2,3 . Here, we investigate the sensory representation (visual and somatosensory) in the lateral pallium (LPal; cortex) of lamprey, and to what degree it resembles that of mammals. The mammalian neocortex is organised into distinct sensory areas, including retinotopic visual and somatotopic somatosensory areas, as well as motor areas. This has been thought to be unique and an evolutionarily recent innovation in mammals [4][5][6][7] . The primary visual area in mammals receives input from the retina, relayed via the lateral geniculate nucleus. In addition, visual information from the superior colliculus is relayed via thalamus to neocortex 8,9 . Somatosensory information is mediated through the lemniscal input to cortical somatosensory areas via the ventral posterior nucleus of thalamus [10][11][12] .In non-mammalian amniotes (reptiles and birds), pallium receives visual, somatosensory and auditory inputs relayed via thalamus 5,6 . In turtles, the three-layered dorsal cortex has a visual representation, however, reported not to be organised in a retinotopic fashion 13 . Much less is known about the somatosensory organisation in the reptilian dorsal cortex 14 . In birds, visual
Dopamine neurons in the SNc play a pivotal role in modulating motor behavior via striatum. Here, we show that the same dopamine neuron that targets striatum also sends a direct branch to the optic tectum (superior colliculus). Whenever SNc neurons are activated, both targets will therefore be affected. Visual stimuli (looming or bars) activate the dopamine neurons coding saliency and also elicit distinct motor responses mediated via tectum (eye, orienting or evasive), which are modulated by the dopamine input. Whole-cell recordings from tectal projection neurons and interneurons show that dopamine, released by SNc stimulation, increases or decreases the excitability depending on whether they express the dopamine D1 or the D2 receptor. SNc thus exerts its effects on the visuomotor system through a combined effect directly on tectum and also via striatum. This direct SNc modulation will occur regardless of striatum and represents a novel mode of motor control.
Animals integrate the different senses to facilitate event-detection for navigation in their environment. In vertebrates, the optic tectum (superior colliculus) commands gaze shifts by synaptic integration of different sensory modalities. Recent works suggest that tectum can elaborate gaze reorientation commands on its own, rather than merely acting as a relay from upstream/forebrain circuits to downstream premotor centers. We show that tectal circuits can perform multisensory computations independently and, hence, configure final motor commands. Single tectal neurons receive converging visual and electrosensory inputs, as investigated in the lamprey - a phylogenetically conserved vertebrate. When these two sensory inputs overlap in space and time, response enhancement of output neurons occurs locally in the tectum, whereas surrounding areas and temporally misaligned inputs are inhibited. Retinal and electrosensory afferents elicit local monosynaptic excitation, quickly followed by inhibition via recruitment of GABAergic interneurons. Multisensory inputs can thus regulate event-detection within tectum through local inhibition without forebrain control.DOI: http://dx.doi.org/10.7554/eLife.16472.001
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