scholarly journals The neural bases of vertebrate motor behaviour through the lens of evolution

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’.

Author(s):  
Paul S. Katz ◽  
Akira Sakurai

This article compares the neural basis for swimming in sea slugs belonging to the Nudipleura clade of molluscs. There are two primary forms of swimming. One, dorsal/ventral (DV) body flexions, is typified by Tritonia diomedea and Pleurobranchaea californica. Although Tritonia and Pleurobranchaea evolved DV swimming independently, there are at least two homologous neurons in the central pattern generators (CPGs) underlying DV swimming in these species. Furthermore, both species have serotonergic neuromodulation of synaptic strength intrinsic to their CPGs. The other form of swimming is with alternating left/right (LR) body flexions. Melibe and Dendronotus belong to a clade of species that all swim with LR body flexions. Although the swimming behavior is homologous, their swim CPGs differ in both cellular composition and in the details of the neural mechanisms. Thus, similar behaviors have independently evolved through parallel use of homologous neurons, and homologous behaviors can be produced by different neural mechanisms.


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):  
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’.


2017 ◽  
Vol 27 (2) ◽  
pp. 40
Author(s):  
Hua WU ◽  
Zaihua RU ◽  
Congying XU ◽  
Xudong GU ◽  
Jianming FU

Author(s):  
Astrid A. Prinz

This chapter begins by defining central pattern generators (CPGs) and proceeds to focus on one of their core components, the timing circuit. After arguing why invertebrate CPGs are particularly useful for the study of neuronal circuit operation in general, the bulk of the chapter then describes basic mechanisms of CPG operation at the cellular, synaptic, and network levels, and how different CPGs combine these mechanisms in various ways. Finally, the chapter takes a semihistorical perspective to discuss whether or not the study of invertebrate CPGs has seen its prime and what it has contributed—and may continue to offer—to a wider understanding of neuronal circuits in general.


2020 ◽  
Vol 375 (1796) ◽  
pp. 20190319 ◽  
Author(s):  
Claus C. Hilgetag ◽  
Alexandros Goulas

Concepts shape the interpretation of facts. One of the most popular concepts in systems neuroscience is that of ‘hierarchy’. However, this concept has been interpreted in many different ways, which are not well aligned. This observation suggests that the concept is ill defined. Using the example of the organization of the primate visual cortical system, we explore several contexts in which ‘hierarchy’ is currently used in the description of brain networks. We distinguish at least four different uses, specifically, ‘hierarchy’ as a topological sequence of projections, as a gradient of features, as a progression of scales, or as a sorting of laminar projection patterns. We discuss the interpretation and functional implications of the different notions of ‘hierarchy’ in these contexts and suggest that more specific terms than ‘hierarchy’ should be used for a deeper understanding of the different dimensions of the organization of brain networks. This article is part of the theme issue ‘Unifying the essential concepts of biological networks: biological insights and philosophical foundations’.


2001 ◽  
Vol 42 (4) ◽  
pp. 291-326 ◽  
Author(s):  
Pietro-Luciano Buono ◽  
Martin Golubitsky

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