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![Integration of vision and electroreception in the deep layer of the lamprey optic tectum. (A) Inset i: Schematic of the lamprey brain showing the visual (blue) and electrosensory (red) afferents targeting the optic tectum (OT). Inset ii: Photomicrograph of the optic tectum in a transversal view showing the retinal afferents reaching the most superficial layers (red), and the octavolateral fibers innervating the intermediate layers (green). Inset iii: Morphology of an output neuron in the deep layer retrogradely labeled following a tracer injection in the middle rhombencephalic reticulospinal nucleus (MRRN) and filled intracellularly with Neurobiotin while performing whole-cell recordings. Output cells extend their dendrites to the intermediate and superficial layers where the electrosensory and the visual inputs enter and terminate, respectively. Abbreviations: SL, superficial layer; IntL, intermediate layer; DL, deep layer. Scale bars: Inset ii, 100 mm; Inset iii, 50 mm. (B) Experimental settings for performing extracellular recordings during multisensory integration in the optic tectum. Dorsal view of the preparation, including the brain, the eyes and electrosensory areas (depicted by the skin patches; for more information see Bodznick and Preston [1983]), while driving output activity with light and electrical stimuli that are spatiotemporally aligned in the immediate surrounding. Abbreviations: rec: extracellular recording electrode. (C) Rectified local field potentials obtained from visual (inset i), electrosensory (inset ii) and bimodal sensory activation (inset iii). Upper traces show sensory stimulation before (black), and after local application of 10 mM gabazine (green). Horizontal dotted lines illustrate the level of peak activity during control. (D) Sensory response against stimulus duration (50-1000 ms) for visual, electroreceptive and bimodal activation, with and without local inhibition. The integral under the curve of rectified local field potentials, as those shown in C, is plotted on the y-axis and normalized to the maximum bimodal response measured during control (n = 13). Paired t-test gave statistical significance as indicated (**p<0.01, ***p<0.001). DOI: 10.7554/eLife.16472.004 The following figure supplement is available for figure 1: Figure supplement 1. Actual responses against the predicted arithmetic sum of unisensory responses. DOI: 10.7554/eLife.16472.005](profile/Juan-Perez-Fernandez-2/publication/320689117/figure/fig1/AS:554434603294720@1509198918504/Integration-of-vision-and-electroreception-in-the-deep-layer-of-the-lamprey-optic-tectum.png)
Integration of vision and electroreception in the deep layer of the lamprey optic tectum. (A) Inset i: Schematic of the lamprey brain showing the visual (blue) and electrosensory (red) afferents targeting the optic tectum (OT). Inset ii: Photomicrograph of the optic tectum in a transversal view showing the retinal afferents reaching the most superficial layers (red), and the octavolateral fibers innervating the intermediate layers (green). Inset iii: Morphology of an output neuron in the deep layer retrogradely labeled following a tracer injection in the middle rhombencephalic reticulospinal nucleus (MRRN) and filled intracellularly with Neurobiotin while performing whole-cell recordings. Output cells extend their dendrites to the intermediate and superficial layers where the electrosensory and the visual inputs enter and terminate, respectively. Abbreviations: SL, superficial layer; IntL, intermediate layer; DL, deep layer. Scale bars: Inset ii, 100 mm; Inset iii, 50 mm. (B) Experimental settings for performing extracellular recordings during multisensory integration in the optic tectum. Dorsal view of the preparation, including the brain, the eyes and electrosensory areas (depicted by the skin patches; for more information see Bodznick and Preston [1983]), while driving output activity with light and electrical stimuli that are spatiotemporally aligned in the immediate surrounding. Abbreviations: rec: extracellular recording electrode. (C) Rectified local field potentials obtained from visual (inset i), electrosensory (inset ii) and bimodal sensory activation (inset iii). Upper traces show sensory stimulation before (black), and after local application of 10 mM gabazine (green). Horizontal dotted lines illustrate the level of peak activity during control. (D) Sensory response against stimulus duration (50-1000 ms) for visual, electroreceptive and bimodal activation, with and without local inhibition. The integral under the curve of rectified local field potentials, as those shown in C, is plotted on the y-axis and normalized to the maximum bimodal response measured during control (n = 13). Paired t-test gave statistical significance as indicated (**p<0.01, ***p<0.001). DOI: 10.7554/eLife.16472.004 The following figure supplement is available for figure 1: Figure supplement 1. Actual responses against the predicted arithmetic sum of unisensory responses. DOI: 10.7554/eLife.16472.005
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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 actin...
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... 3 From the lamprey to primates, OT has formed and existed for millions of years, while still exhibiting striking similarities in its fundamental functions, layered organization, and cellular composition. 11 In fish, OT located in the midbrain constitutes a substantial portion of the brain, serving as the main visual center where the majority of optic fibers terminate. 12 During evolution, the OT has gradually developed a layered structure exhibiting enhanced clarity and precision. ...
The avian optic tectum (OT) has been studied for its diverse functions, yet a comprehensive molecular landscape at the cellular level has been lacking. In this study, we applied spatial transcriptome sequencing and single-nucleus RNA sequencing (snRNA-seq) to explore the cellular organization and molecular characteristics of the avian OT from two species: Columba livia and Taeniopygia guttata. We identified precise layer structures and provided comprehensive layer-specific signatures of avian OT. Furthermore, we elucidated diverse functions in different layers, with the stratum griseum periventriculare (SGP) potentially playing a key role in advanced functions of OT, like fear response and associative learning. We characterized detailed neuronal subtypes and identified a population of FOXG1+ excitatory neurons, resembling those found in the mouse neocortex, potentially involved in neocortex-related functions and expansion of avian OT. These findings could contribute to our understanding of the architecture of OT, shedding light on visual perception and multifunctional association.
... Human eyes comprise a unique tool for social communications due to their morphological feature (Kobayashi and Kohshima, 1997); the exposed white sclera surrounds the dark iris, making it easier for others to detect what the subject is looking. The "eye contact" tactics could therefore be unique to humans, despite the subcortical pathway underlying orienting gaze control is evolutionarily conserved (Dean et al., 1989;Kardamakis et al., 2016). This morphology makes "eye contact" a powerful means to communicate socially in typically developing people, whereas adults with ASD often report adverse emotional responses to looking eyes of others and avoid "eye contact" (Trevisan et al., 2017). ...
Equipped with an early social predisposition immediately post-birth, humans typically form associations with mothers and other family members through exposure learning, canalized by a prenatally formed predisposition of visual preference to biological motion, face configuration, and other cues of animacy. If impaired, reduced preferences can lead to social interaction impairments such as autism spectrum disorder (ASD) via misguided canalization. Despite being taxonomically distant, domestic chicks could also follow a homologous developmental trajectory toward adaptive socialization through imprinting, which is guided via predisposed preferences similar to those of humans, thereby suggesting that chicks are a valid animal model of ASD. In addition to the phenotypic similarities in predisposition with human newborns, accumulating evidence on the responsible molecular mechanisms suggests the construct validity of the chick model. Considering the recent progress in the evo-devo studies in vertebrates, we reviewed the advantages and limitations of the chick model of developmental mental diseases in humans.
... Lampreys also possess the main centers involved in goaloriented gaze redirection. As in mammals, the optic tectum (OT; mammalian superior colliculus) has a layered structure and receives visual information retinotopically, aligned with other sensory modalities (de Arriba Mdel and Pombal, 2007;Jones et al., 2009;Cornide-Petronio et al., 2011;Kardamakis et al., 2016). Sensory information is integrated by the tectal circuits that prioritize salient stimuli and encode the appropriate behavioral response by generating orienting/evasive movements (Saitoh et al., 2007;Kardamakis et al., 2015;Kardamakis et al., 2016;Kardamakis et al., 2017;Suzuki et al., 2019). ...
... As in mammals, the optic tectum (OT; mammalian superior colliculus) has a layered structure and receives visual information retinotopically, aligned with other sensory modalities (de Arriba Mdel and Pombal, 2007;Jones et al., 2009;Cornide-Petronio et al., 2011;Kardamakis et al., 2016). Sensory information is integrated by the tectal circuits that prioritize salient stimuli and encode the appropriate behavioral response by generating orienting/evasive movements (Saitoh et al., 2007;Kardamakis et al., 2015;Kardamakis et al., 2016;Kardamakis et al., 2017;Suzuki et al., 2019). The OT also receives other inputs that can modulate its motor commands, including those from the basal ganglia and cortex (Stephenson-Jones et al., 2011;Pérez-Fernández et al., 2014;Pérez-Fernández et al., 2017;Pérez-Fernández et al., 2021;Ocaña et al., 2015). ...
... Although the order of appearance of the different visual components, and the development of the retinofugal pathways have been described (Kennedy and Rubinson, 1977;de Miguel et al., 1990;Cornide-Petronio et al., 2011), their functionality is unknown. Moreover, although some of the motor pathways that generate orienting, evasive, and eye movements are well described in adults (Saitoh et al., 2007;Kardamakis et al., 2015;Kardamakis et al., 2016;Kardamakis et al., 2017;Suzuki et al., 2019), their development is still unknown. In this study, we show that larval lampreys have coordinated eye movements in the form of VOR, and that eye movements can also be evoked by light stimuli. ...
Animals constantly redirect their gaze away or towards relevant targets and, besides these goal-oriented responses, stabilizing movements clamp the visual scene avoiding image blurring. The vestibulo-ocular (VOR) and the optokinetic reflexes are the main contributors to gaze stabilization, whereas the optic tectum integrates multisensory information and generates orienting/evasive gaze movements in all vertebrates. Lampreys show a unique stepwise development of the visual system whose understanding provides important insights into the evolution and development of vertebrate vision. Although the developmental emergence of the visual components, and the retinofugal pathways have been described, the functional development of the visual system and the development of the downstream pathways controlling gaze are still unknown. Here, we show that VOR followed by light-evoked eye movements are the first to appear already in larvae, despite their burrowed lifestyle. However, the circuits controlling goal-oriented responses emerge later, in larvae in non-parasitic lampreys but during late metamorphosis in parasitic lampreys. The appearance of stabilizing responses earlier than goal-oriented in the lamprey development shows a stepwise transition from simpler to more complex visual systems, offering a unique opportunity to isolate the functioning of their underlying circuits.
... Although surround modulation is observed across both visual thalamocortical in the lateral geniculate nucleus (Bonin et al., 2005), primary visual cortex (Jones et al., 2001) and extrastriate cortex (Born & Bradley, 2005), and in retinotectal systems in the optic tectum (Fernandes et al., 2021;Kardamakis et al., 2015Kardamakis et al., , 2016 or superior colliculus (Kasai & Isa, 2016;Schiller & Koerner, 1971), its origin in the retina (Flores-Herr et al., 2001;Kim et al., 2022;Solomon et al., 2006;Y. Zhang et al., 2012) suggests that certain effects are likely fed forward to later stages of the visual hierarchy. ...
Extraretinal circuits can shape visual center-surround interactions that originate in the retina, yet the contributing circuit mechanisms to this initial modulation remain elusive. Using an optogenetic-based approach applied to the superficial layers of the superior colliculus (SCs), we demonstrate that the SCs is sufficient in generating surround suppression through selective patterned activation of visual center and surround zones in individual neurons. Like in the primary visual cortex, surround network activation causes decreases in center excitation rather than increases in synaptic inhibition. We reveal the identity of a SCs-based circuit with two interacting circuit motifs, recurrent excitation and feedback inhibition, capable of modulating levels of center excitation when the visual surround is active, using whole-cell recordings, trans-synaptic mapping, and functional approaches with computational modeling. We propose that early subcortical and cortical visual circuits have evolved to perform surround modulation independently, thereby enhancing visuospatial versatility across multiple levels.
... Whether lampreys have optokinetic eye movements is still unclear. The fact that they have retinotopic representation in both tectum and visual cortex, and a precise control of eye movements from tectum suggests that vision may contribute to gaze stabilization [21][22][23][24][25][26] . ...
... The anatomical results and data in other vertebrates suggested that pretectum is the primary contributor of visual information to OKR 8,9 . However, tectum plays a key role in visual processing [21][22][23]25 and therefore we aimed to identify which region is the primary contributor. We complemented the tracer injections with acute inactivation of these two brain areas to see the impact on the dorsal rectus activity evoked by optokinetic stimulation. ...
... The clear interconnectivity between pretectal, vestibular, and oculomotor nuclei also supports the notion that both OKR and VOR are of subcortical origins, highlighting a principal role of subcortical mechanisms, which has likely been maintained in mammals due to the phylogenetic preservation of the visual system 15,23,25,26 . The absence of a functional cerebellum in lampreys shows that cerebellar pathways are not needed for the OKR. ...
Gaze stabilization compensates for movements of the head or external environment to minimize image blurring. Multisensory information stabilizes the scene on the retina via the vestibulo-ocular (VOR) and optokinetic (OKR) reflexes. While the organization of neuronal circuits underlying VOR is well-described across vertebrates, less is known about the contribution and evolution of the OKR and the basic structures allowing visuo-vestibular integration. To analyze these neuronal pathways underlying visuo-vestibular integration, we developed a setup using a lamprey eye-brain-labyrinth preparation, which allowed coordinating electrophysiological recordings, vestibular stimulation with a moving platform, and visual stimulation via screens. Lampreys exhibit robust visuo-vestibular integration, with optokinetic information processed in the pretectum that can be downregulated from tectum. Visual and vestibular inputs are integrated at several subcortical levels. Additionally, saccades are present in the form of nystagmus. Thus, all basic components of the visuo-vestibular control of gaze were present already at the dawn of vertebrate evolution.
... For example, Key (2015) points out three features; subregionalization including mapped sensorimotor representations, laminated cytoarchitecture, and columnar microcircuits. However, all of these features are also found in non-cortical regions, especially in the midbrain tectum (superior colliculus in mammals) (Feinberg and Mallatt 2016a, Kardamakis et al. 2015Kardamakis et al. , 2016Kardamakis et al. , 2018Masullo et al. 2019;Suzuki and Grillner 2018). Therefore, it appears to be a preconception to believe that there should be some quintessence of consciousness found only in the cortex and its counterparts. ...
The evolutionary origin(s) of consciousness has been a growing area of study in recent years. Nevertheless, there is intense debate on whether the existence of phenomenal consciousness without the cerebral cortex is possible. The corticocentrists have an empirical advantage because we are quasi-confident that we humans are conscious and have the well-developed cortex as the site of our consciousness. However, their prejudice can be an anthropic bias similar to the anthropocentric prejudice in pre-Darwinian natural history. In this paper, I propose three basic principles to provide a conceptual basis for evolutionary studies of consciousness: the non-solipsistic principle, the evolution principle, and the anthropic principle. These principles collectively help us to avoid solipsism, anthropocentrism, and anthropomorphism to some degree, although we cannot be completely free from them. Also, the landscape metaphor associated with the anthropic principle provides an image of how different forms of consciousness can be acquired.
... Multisensory integration can lead to responses that are comparable, weaker or greater than the sum of the individual responses (Meredith and Stein, 1986;Stein and Stanford, 2008;Stein et al., 2009Stein et al., , 2014. Excitatory inputs activating NMDA-type glutamate receptors and local or global inhibitory feedback can both contribute to the nonlinear nature of multimodal enhancement (Meredith et al., 1987;Binns and Salt, 1996;Stein and Stanford, 2008;Zahar et al., 2009;Cuppini et al., 2010;Harwell et al., 2015;Felch et al., 2016;Kardamakis et al., 2016;Truszkowski et al., 2017). ...
... Few studies elucidate mechanisms of multimodal integration on the cellular level (Felch et al., 2016;Kardamakis et al., 2016;Truszkowski et al., 2017). The Shepherd's crook neuron (SCN) with its unique morphology offers an ideal basis to study these principles in single multimodal neurons. ...
... Inhibitory feedback is necessary for multimodal integration (Friedel and van Hemmen, 2008;Cuppini et al., 2010;Stein et al., 2014;Felch et al., 2016;Kardamakis et al., 2016;Miller et al., 2017). We included feedforward inhibition converging onto the SCN neuron in the model by placing a total of four conductance point sources (ExpSyn mechanism) on the distal dendritic compartments (at 0.4 compartment lengths; g syn : 1 nS per synapse, t decay : 75 ms, E rev : -85 mV). ...
Multimodal integration facilitates object recognition and response to sensory cues. This depends on spatio-temporal coincidence of sensory information, recruitment of NMDA-type glutamate receptors and inhibitory feedback. Shepherd's crook neurons in the avian optic tectum are an ideal model for studying cellular mechanism of multimodal integration. They receive different sensory modalities through spatially segregated dendrites, are important for stimulus selection and have an axon-carrying dendrite. We performed whole-cell patch-clamp experiments in chicken midbrain slices of both sexes. We emulated visual and auditory input in vitro by stimulating presynaptic afferents electrically. Simultaneous stimulation enhanced responses inversely depending on stimulation amplitude demonstrating the principle of inverse effectiveness. Contribution of NMDA-type glutamate receptors prolonged postsynaptic events for visual inputs only, causing a strong modality-specific difference in synaptic efficacy. We designed a multi-compartment model to study the effect of morphological and physiological parameters on multimodal integration by varying the distance between soma and axonal origin and the amount of NMDAR contribution. These parameters changed the preference of the model for one input channel and adjusted the range of input rates at which multimodal enhancement occurred upon naturalistic stimulation. Thus, the unique morphology and synaptic features of Shepherd's crook neurons shape the integration of input at different dendrites and generates an enhanced multimodal response.
... In a somewhat deeper layer, other senses provide maps aligned spatially with the visual map, such as electrosensation in the lamprey or auditory stimuli in mammals. Input originating from the same location in space provided from two different senses facilitate each other, and if instead they are in conflict, they inhibit each other both in the lamprey and in rodents [15,[30][31][32]. The aligned spatial information from a given point in space will directly or indirectly excite the tectal output neurons, while at the same time they inhibit neurons in the surrounding tectal area with a form of lateral inhibition. ...
The primary driver of the evolution of the vertebrate nervous system has been the necessity to move, along with the requirement of controlling the plethora of motor behavioural repertoires seen among the vast and diverse vertebrate species. Understanding the neural basis of motor control through the perspective of evolution, mandates thorough examinations of the nervous systems of species in critical phylogenetic positions. We present here, a broad review of studies on the neural motor infrastructure of the lamprey, a basal and ancient vertebrate, which enjoys a unique phylogenetic position as being an extant representative of the earliest group of vertebrates. From the central pattern generators in the spinal cord to the microcircuits of the pallial cortex, work on the lamprey brain over the years, has provided detailed insights into the basic organization (a bauplan) of the ancestral vertebrate brain, and narrates a compelling account of common ancestry of fundamental aspects of the neural bases for motion control, maintained through half a billion years of vertebrate evolution.
This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.
... The lamprey, a jawless vertebrate which diverged from the vertebrate evolutionary line 560 million years ago, features a nervous system which in many ways is representative of that seen in mammals 76 In contrast, it is unclear whether lamprey possess an OKR. Its visual system is, as previously noted, well-developed, and its optic tectum corresponds to the mammalian superior colliculus in its function of dictating gaze shifts based on multisensory input 81 . Much like its human homologue, the optic tectum is layered, and its superficial segment receives visual information from the retina according to a retinotopic map 78 . ...
... Additionally, the SNc/VTA receives inputs from other sensory regions. This includes the octavolateral area [3], a region that integrates mechanosensory, electrosensory, and vestibular information [51,52], and the dorsal column nucleus, which receives mechanosensory information from the spinal cord. Other evolutionarily conserved inputs to the SNc/VTA include projections from the cortical homologue (pallium), habenula, thalamus, and pedunculopontine nucleus (Figure 2a) [3]. ...
... Neurons in the deep layer subsequently project contra-or ipsi-laterally to the brainstem to evoke orienting or evasive responses, respectively. Additionally, visual inputs activate interneurons that provide lateral feedforward inhibition that silences competing areas, which in turn allows for stimulus selection [51,[63][64][65]. This architecture is very similar to that observed in the tectum/SC of other vertebrate groups, including mammals, indicating a large degree of conservation [66]. ...
Dopamine is likely the most studied modulatory neurotransmitter, in great part due to characteristic motor deficits in Parkinson’s disease that arise after the degeneration of the dopaminergic neurons in the substantia nigra pars compacta (SNc). The SNc, together with the ventral tegmental area (VTA), play a key role modulating motor responses through the basal ganglia. In contrast to the large amount of existing literature addressing the mammalian dopaminergic system, comparatively little is known in other vertebrate groups. However, in the last several years, numerous studies have been carried out in basal vertebrates, allowing a better understanding of the evolution of the dopaminergic system, especially the SNc/VTA. We provide an overview of existing research in basal vertebrates, mainly focusing on lampreys, belonging to the oldest group of extant vertebrates. The lamprey dopaminergic system and its role in modulating motor responses have been characterized in significant detail, both anatomically and functionally, providing the basis for understanding the evolution of the SNc/VTA in vertebrates. When considered alongside results from other early vertebrates, data in lampreys show that the key role of the SNc/VTA dopaminergic neurons modulating motor responses through the basal ganglia was already well developed early in vertebrate evolution.
