scholarly journals The neuroecology of the water-to-land transition and the evolution of the vertebrate brain

Author(s):  
Malcolm A. MacIver ◽  
Barbara L. Finlay

The water-to-land transition in vertebrate evolution offers an unusual opportunity to consider computational affordances of a new ecology for the brain. All sensory modalities are changed, particularly a greatly enlarged visual sensorium owing to air versus water as a medium, and expanded by mobile eyes and neck. The multiplication of limbs, as evolved to exploit aspects of life on land, is a comparable computational challenge. As the total mass of living organisms on land is a hundredfold larger than the mass underwater, computational improvements promise great rewards. In water, the midbrain tectum coordinates approach/avoid decisions, contextualized by water flow and by the animal’s body state and learning. On land, the relative motions of sensory surfaces and effectors must be resolved, adding on computational architectures from the dorsal pallium, such as the parietal cortex. For the large-brained and long-living denizens of land, making the right decision when the wrong one means death may be the basis of planning, which allows animals to learn from hypothetical experience before enactment. Integration of value-weighted, memorized panoramas in basal ganglia/frontal cortex circuitry, with allocentric cognitive maps of the hippocampus and its associated cortices becomes a cognitive habit-to-plan transition as substantial as the change in ecology. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

Author(s):  
David A. Leopold ◽  
Bruno B. Averbeck

We are curious by nature, particularly when young. Evolution has endowed our brain with an inbuilt obligation to educate itself. In this perspectives article, we posit that self-tuition is an evolved principle of vertebrate brain design that is reflected in its basic architecture and critical for its normal development. Self-tuition involves coordination between functionally distinct components of the brain, with one set of areas motivating exploration that leads to the experiences that train another set. We review key hypothalamic and telencephalic structures involved in this interplay, including their anatomical connections and placement within the segmental architecture of conserved forebrain circuits. We discuss the nature of educative behaviours motivated by the hypothalamus, innate stimulus biases, the relationship to survival in early life, and mechanisms by which telencephalic areas gradually accumulate knowledge. We argue that this aspect of brain function is of paramount importance for systems neuroscience, as it confers neural specialization and allows animals to attain far more sophisticated behaviours than would be possible through genetic mechanisms alone. Self-tuition is of particular importance in humans and other primates, whose large brains and complex social cognition rely critically on experience-based learning during a protracted childhood period. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.


Author(s):  
Shreyas M. Suryanarayana ◽  
Brita Robertson ◽  
Sten Grillner

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’.


2008 ◽  
Vol 364 (1519) ◽  
pp. 1021-1032 ◽  
Author(s):  
Lucilla Facchin ◽  
Harold A Burgess ◽  
Mahmud Siddiqi ◽  
Michael Granato ◽  
Marnie E Halpern

As in many fishes, amphibians and reptiles, the epithalamus of the zebrafish, Danio rerio , develops with pronounced left–right (L–R) asymmetry. For example, in more than 95 per cent of zebrafish larvae, the parapineal, an accessory to the pineal organ, forms on the left side of the brain and the adjacent left habenular nucleus is larger than the right. Disruption of Nodal signalling affects this bias, producing equal numbers of larvae with the parapineal on the left or the right side and corresponding habenular reversals. Pre-selection of live larvae using fluorescent transgenic reporters provides a useful substrate for studying the effects of neuroanatomical asymmetry on behaviour. Previous studies had suggested that epithalamic directionality is correlated with lateralized behaviours such as L–R eye preference. We find that the randomization of epithalamic asymmetry, through perturbation of the nodal -related gene southpaw , does not alter a variety of motor behaviours, including responses to lateralized stimuli. However, we discovered significant deficits in swimming initiation and in the total distance navigated by larvae with parapineal reversals. We discuss these findings with respect to previous studies and recent work linking the habenular region with control of the motivation/reward pathway of the vertebrate brain.


2012 ◽  
Vol 2012 ◽  
pp. 1-15 ◽  
Author(s):  
Paula Plaza ◽  
Isabel Cuevas ◽  
Cécile Grandin ◽  
Anne G. De Volder ◽  
Laurent Renier

A visual-to-auditory sensory substitution device initially developed for the blind is known to allow visual-like perception through sequential exploratory strategies. Here we used functional magnetic resonance imaging (fMRI) to test whether processing the location versus the orientation of simple (elementary) “visual” stimuli encoded into sounds using the device modulates the brain activity within the dorsal visual stream in the absence of sequential exploration of these stimuli. Location and orientation detection with the device induced a similar recruitment of frontoparietal brain areas in blindfolded sighted subjects as the corresponding tasks using the same stimuli in the same subjects in vision. We observed a similar preference of the right superior parietal lobule for spatial localization over orientation processing in both sensory modalities. This provides evidence that the parietal cortex activation during the use of the prosthesis is task related and further indicates the multisensory recruitment of the dorsal visual pathway in spatial processing.


Author(s):  
Luiz Pessoa ◽  
Loreta Medina ◽  
Ester Desfilis

Mental terms—such as perception, cognition, action, emotion, as well as attention, memory, decision-making—are epistemically sterile. We support our thesis based on extensive comparative neuroanatomy knowledge of the organization of the vertebrate brain. Evolutionary pressures have moulded the central nervous system to promote survival. Careful characterization of the vertebrate brain shows that its architecture supports an enormous amount of communication and integration of signals, especially in birds and mammals. The general architecture supports a degree of ‘computational flexibility’ that enables animals to cope successfully with complex and ever-changing environments. Here, we suggest that the vertebrate neuroarchitecture does not respect the boundaries of standard mental terms, and propose that neuroscience should aim to unravel the dynamic coupling between large-scale brain circuits and complex, naturalistic behaviours. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.


2018 ◽  
Vol 29 (9) ◽  
pp. 3590-3605 ◽  
Author(s):  
Jodie Davies-Thompson ◽  
Giulia V Elli ◽  
Mohamed Rezk ◽  
Stefania Benetti ◽  
Markus van Ackeren ◽  
...  

Abstract The brain has separate specialized computational units to process faces and voices located in occipital and temporal cortices. However, humans seamlessly integrate signals from the faces and voices of others for optimal social interaction. How are emotional expressions, when delivered by different sensory modalities (faces and voices), integrated in the brain? In this study, we characterized the brains’ response to faces, voices, and combined face–voice information (congruent, incongruent), which varied in expression (neutral, fearful). Using a whole-brain approach, we found that only the right posterior superior temporal sulcus (rpSTS) responded more to bimodal stimuli than to face or voice alone but only when the stimuli contained emotional expression. Face- and voice-selective regions of interest, extracted from independent functional localizers, similarly revealed multisensory integration in the face-selective rpSTS only; further, this was the only face-selective region that also responded significantly to voices. Dynamic causal modeling revealed that the rpSTS receives unidirectional information from the face-selective fusiform face area, and voice-selective temporal voice area, with emotional expression affecting the connection strength. Our study promotes a hierarchical model of face and voice integration, with convergence in the rpSTS, and that such integration depends on the (emotional) salience of the stimuli.


Author(s):  
Justin M. Fine ◽  
Benjamin Y. Hayden

We propose that the entirety of the prefrontal cortex (PFC) can be seen as fundamentally premotor in nature. By this, we mean that the PFC consists of an action abstraction hierarchy whose core function is the potentiation and depotentiation of possible action plans at different levels of granularity. We argue that the apex of the hierarchy should revolve around the process of goal-selection, which we posit is inherently a form of optimization over action abstraction. Anatomical and functional evidence supports the idea that this hierarchy originates on the orbital surface of the brain and extends dorsally to motor cortex. Accordingly, our viewpoint positions the orbitofrontal cortex in a key role in the optimization of goal-selection policies, and suggests that its other proposed roles are aspects of this more general function. Our proposed perspective will reframe outstanding questions, open up new areas of inquiry and align theories of prefrontal function with evolutionary principles. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.


2017 ◽  
Author(s):  
Jodie Davies-Thompson ◽  
Giulia V. Elli ◽  
Mohamed Rezk ◽  
Stefania Benetti ◽  
Markus van Ackeren ◽  
...  

ABSTRACTThe brain has separate specialized computational units to process faces and voices located in occipital and temporal cortices. However, humans seamlessly integrate signals from the faces and voices of others for optimal social interaction. How are emotional expressions, when delivered by different sensory modalities (faces and voices), integrated in the brain? In this study, we characterized the brains’ response to faces, voices, and combined face-voice information (congruent, incongruent), which varied in expression (neutral, fearful). Using a whole-brain approach, we found that only the right posterior superior temporal sulcus (rpSTS) responded more to bimodal stimuli than to face or voice alone but only when the stimuli contained emotional expression. Face-and voice-selective regions of interest extracted from independent functional localizers, similarly revealed multisensory integration in the face-selective rpSTS only; further, this was the only face-selective region that also responded significantly to voices. Dynamic Causal Modeling revealed that the rpSTS receives unidirectional information from the face-selective fusiform face area (FFA), and voice-selective temporal voice area (TVA), with emotional expression affecting the connection strength. Our study promotes a hierarchical model of face and voice integration, with convergence in the rpSTS, and that such integration depends on the (emotional) salience of the stimuli.


Author(s):  
Paul Cisek ◽  
Benjamin Y. Hayden

The nervous system is a product of evolution. That is, it was constructed through a long series of modifications, within the strong constraints of heredity, and continuously subjected to intense selection pressures. As a result, the organization and functions of the brain are shaped by its history. We believe that this fact, underappreciated in contemporary systems neuroscience, offers an invaluable aid for helping us resolve the brain's mysteries. Indeed, we think that the consideration of evolutionary history ought to take its place alongside other intellectual tools used to understand the brain, such as behavioural experiments, studies of anatomical structure and functional characterization based on recordings of neural activity. In this introduction, we argue for the importance of evolution by highlighting specific examples of ways that evolutionary theory can enhance neuroscience. The rest of the theme issue elaborates this point, emphasizing the conservative nature of neural evolution, the important consequences of specific transitions that occurred in our history, and the ways in which considerations of evolution can shed light on issues ranging from specific mechanisms to fundamental principles of brain organization. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.


Author(s):  
M. Sato ◽  
Y. Ogawa ◽  
M. Sasaki ◽  
T. Matsuo

A virgin female of the noctuid moth, a kind of noctuidae that eats cucumis, etc. performs calling at a fixed time of each day, depending on the length of a day. The photoreceptors that induce this calling are located around the neurosecretory cells (NSC) in the central portion of the protocerebrum. Besides, it is considered that the female’s biological clock is located also in the cerebral lobe. In order to elucidate the calling and the function of the biological clock, it is necessary to clarify the basic structure of the brain. The observation results of 12 or 30 day-old noctuid moths showed that their brains are basically composed of an outer and an inner portion-neural lamella (about 2.5 μm) of collagen fibril and perineurium cells. Furthermore, nerve cells surround the cerebral lobes, in which NSCs, mushroom bodies, and central nerve cells, etc. are observed. The NSCs are large-sized (20 to 30 μm dia.) cells, which are located in the pons intercerebralis of the head section and at the rear of the mushroom body (two each on the right and left). Furthermore, the cells were classified into two types: one having many free ribosoms 15 to 20 nm in dia. and the other having granules 150 to 350 nm in dia. (Fig. 1).


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