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

Ocaña, Francisco M.; Suryanarayana, Shreyas M.; Saitoh, Ken-ichi; Kardamakis, Andreas A.; Capantini, Lorenza; Robertson, Brita; Grillner, Sten

doi:10.1016/j.cub.2014.12.013

Cited by 81 publications

(91 citation statements)

References 46 publications

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“…Afferents from cortex (pallium in nonmammals) thus provide monosynaptic excitation to tectal output cells in lamprey (Fig. 8D) as in other species (54)(55)(56). Furthermore, the basal ganglia output nuclei instead provide tonic GABAergic inhibition to the tectal output cells in lamprey as well as in mammals (31,(57)(58)(59).…”

Section: Discussionmentioning

confidence: 98%

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

Kardamakis

Saitoh

Grillner

2015

Proc. Natl. Acad. Sci. U.S.A.

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132

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The optic tectum (called superior colliculus in mammals) is critical for eye-head gaze shifts as we navigate in the terrain and need to adapt our movements to the visual scene. The neuronal mechanisms underlying the tectal contribution to stimulus selection and gaze reorientation remains, however, unclear at the microcircuit level. To analyze this complex-yet phylogenetically conservedsensorimotor system, we developed a novel in vitro preparation in the lamprey that maintains the eye and midbrain intact and allows for whole-cell recordings from prelabeled tectal gaze-controlling cells in the deep layer, while visual stimuli are delivered. We found that receptive field activation of these cells provide monosynaptic retinal excitation followed by local GABAergic inhibition (feedforward). The entire remaining retina, on the other hand, elicits only inhibition (surround inhibition). If two stimuli are delivered simultaneously, one inside and one outside the receptive field, the former excitatory response is suppressed. When local inhibition is pharmacologically blocked, the suppression induced by competing stimuli is canceled. We suggest that this rivalry between visual areas across the tectal map is triggered through long-range inhibitory tectal connections. Selection commands conveyed via gazecontrolling neurons in the optic tectum are, thus, formed through synaptic integration of local retinotopic excitation and global tectal inhibition. We anticipate that this mechanism not only exists in lamprey but is also conserved throughout vertebrate evolution.optic tectum | superior colliculus | GABAergic inhibition | gaze control | evolution V isual scenes are composed of abundant stimuli, and the gaze needs continuously to be redirected toward different objectsan important task for the brain. Current models postulate that stimulus selection occurs through a process involving competitive interaction between different visual stimuli, resulting in the appropriate eye-head movement (1-5). The optic tectum (superior colliculus in mammals) has a causal role in the stimulus selection process (6-12) and not only in the control of saccades and eyehead gaze shifts (13-16). Although the collicular contribution to the selection process is of central importance, the underlying neuronal processes have remained elusive due to methodological limitations. It is our aim here to address this issue in a novel experimental model.The optic tectum is well developed in the lamprey, belonging to the oldest extant vertebrate group that evolved 560 million years ago (17), and it has remained conserved throughout vertebrate phylogeny (18)(19)(20)(21)(22). Afferents from retina provide a direct input to the superficial layers of the optic tectum, where a retinotopic map is formed (23-26). The intermediate and deep layers give rise to projections to brainstem areas and a motor map is formed that is responsible for the coordination of eye, head, and body movements (22,(27)(28)(29).To uncover the mechanisms underlying visual stimulus selection for gaz...

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Section: Discussionmentioning

confidence: 98%

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

Kardamakis

Saitoh

Grillner

2015

Proc. Natl. Acad. Sci. U.S.A.

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132

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“…The dorsal pallium gives rise to the majority of the mammalian cerebral neocortex (Medina and Abellán, 2009). Ocaña et al (2015) have recently obtained evidence for functional connectivity between the dorsal and dorsomedial part of lateral pallium and certain brainstem motor centers (pretectum, tectum, midbrain tegmentum and locomotor region, and reticulospinal cells) in lampreys. The brainstem structures they described may correspond to brainstem structures for smooth pursuit eye movements (Mustari et al, 2009) and the pedunculopontine nucleus (PPN, Benarroch, 2013; Gut and Winn, 2016).…”

Section: Evolution To the Human Forebrainmentioning

confidence: 99%

Circuits Regulating Pleasure and Happiness: The Evolution of the Amygdalar-Hippocampal-Habenular Connectivity in Vertebrates

Loonen

Ivanova

2016

Front. Neurosci.

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Appetitive-searching (reward-seeking) and distress-avoiding (misery-fleeing) behavior are essential for all free moving animals to stay alive and to have offspring. Therefore, even the oldest ocean-dwelling animal creatures, living about 560 million years ago and human ancestors, must have been capable of generating these behaviors. The current article describes the evolution of the forebrain with special reference to the development of the misery-fleeing system. Although, the earliest vertebrate ancestor already possessed a dorsal pallium, which corresponds to the human neocortex, the structure and function of the neocortex was acquired quite recently within the mammalian evolutionary line. Up to, and including, amphibians, the dorsal pallium can be considered to be an extension of the medial pallium, which later develops into the hippocampus. The ventral and lateral pallium largely go up into the corticoid part of the amygdala. The striatopallidum of these early vertebrates becomes extended amygdala, consisting of centromedial amygdala (striatum) connected with the bed nucleus of the stria terminalis (pallidum). This amygdaloid system gives output to hypothalamus and brainstem, but also a connection with the cerebral cortex exists, which in part was created after the development of the more recent cerebral neocortex. Apart from bidirectional connectivity with the hippocampal complex, this route can also be considered to be an output channel as the fornix connects the hippocampus with the medial septum, which is the most important input structure of the medial habenula. The medial habenula regulates the activity of midbrain structures adjusting the intensity of the misery-fleeing response. Within the bed nucleus of the stria terminalis the human homolog of the ancient lateral habenula-projecting globus pallidus may exist; this structure is important for the evaluation of efficacy of the reward-seeking response. The described organization offers a framework for the regulation of the stress response, including the medial habenula and the subgenual cingulate cortex, in which dysfunction may explain the major symptoms of mood and anxiety disorders.

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“…Rather, a mutation causing male sterility can spread due to selfish benefits that it alone enjoys, at the expense of the plant carrying it [3]. Male sterility mutations causing gynodioecy very often occur in genes of the mitochondrial genome, which in most flowering plants are transmitted to progeny only through ovules and not through pollen [4,5]. Consequently, these genes have no evolutionary interest at all in the production of pollen, which, from their 'point of view', represents a waste of resources that might otherwise be used to produce more ovules and seeds -this is similar to the advantage gained by male-killing elements in animal species that are transmitted only maternally [5][6][7].…”

Section: Mice Trained To Lick Left or Rightmentioning

confidence: 99%

“…Both intratelencephalic and pyramidal neurons are located in layer 5 of the mammalian cortex, and they have a similar, but not identical, somadendritic morphology. Both types are present throughout vertebrate phylogeny [5].…”

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Action: The Role of Motor Cortex Challenged

Grillner

2015

Current Biology

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

Abstract: Our results demonstrate marked similarities in the efferent functional connectivity and control of motor behavior between the lamprey pallium and mammalian neocortex. Thus, the lamprey motor pallium/cortex represents an evolutionary blueprint of the corresponding mammalian system.

Cited by 81 publications

References 46 publications

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

Circuits Regulating Pleasure and Happiness: The Evolution of the Amygdalar-Hippocampal-Habenular Connectivity in Vertebrates

Action: The Role of Motor Cortex Challenged

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