Abstract
Survival and reproduction entail the selection of adaptive behavioural repertoires. This selection manifests as phylogenetically acquired activities that depend on evolved nervous system circuitries. Lorenz and Tinbergen already postulated that heritable behaviours and their reliable performance are specified by genetically determined programs. Here we compare the functional anatomy of the insect central complex and vertebrate basal ganglia to illustrate their role in mediating selection and maintenance of adaptive behaviours. Comparative analyses reveal that central complex and basal ganglia circuitries share comparable lineage relationships within clusters of functionally integrated neurons. These clusters are specified by genetic mechanisms that link birth time and order to their neuronal identities and functions. Their subsequent connections and associated functions are characterized by similar mechanisms that implement dimensionality reduction and transition through attractor states, whereby spatially organized parallel-projecting loops integrate and convey sensorimotor representations that select and maintain behavioural activity. In both taxa, these neural systems are modulated by dopamine signalling that also mediates memory-like processes. The multiplicity of similarities between central complex and basal ganglia suggests evolutionarily conserved computational mechanisms for action selection. We speculate that these may have originated from ancestral ground pattern circuitries present in the brain of the last common ancestor of insects and vertebrates.
Highlights
Brains of roving animals have evolved to make decisions in response to change in their internal environment based on cues indicative of, for example, nutritional status, and to change in their external environment
The vertebrate basal ganglia (BG) consists of an arrangement of basal forebrain nuclei that includes the striatum, the internal and external domains of the globus pallidus (GPi and GPe, respectively), the subthalamic nucleus (STN), and the substantia nigra pars reticulata (SNr) [11]
To identify the underlying computational mechanisms, we further examined the functional anatomy of CX and BG circuitry
Summary
Brains of roving animals have evolved to make decisions in response to change in their internal environment based on cues indicative of, for example, nutritional status, and to change in their external environment. The vertebrate BG consists of an arrangement of basal forebrain nuclei that includes the striatum (which in primates consists of caudate, putamen and ventral striatum, including nucleus accumbens), the internal and external domains of the globus pallidus (GPi and GPe, respectively), the subthalamic nucleus (STN), and the substantia nigra pars reticulata (SNr) (figure 1b,c) [11] Both the CX and the BG share extensive similarities in their heritable ontogeny and behavioural performance, and previous analyses have identified multiple correspondences between them. These include their embryological derivation and orthologous genetic specification, neural architectures, neurochemical attributes and physiological properties as well as behavioural outcomes of neuronal activity, including pathologies [12,13] Together these correspondences imply a common ancestral origin of circuits that have diverged over a timespan of more than 540 Myr to provide the insect CX and the vertebrate BG. Our analysis suggests that evolutionarily corresponding computational mechanisms underlie the selection and maintenance of adaptive behaviour in insects and vertebrates
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