title: Evolutionarily conserved mechanisms for the selection and maintenance of behavioural activity.
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.
authors.affiliation: Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, London, UK.
authors.forename: Vincenzo G
authors.initials: VG
authors.lastname: Fiore
authors.affiliation: Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, London, UK Max Planck UCL Centre for Computational Psychiatry and Ageing Research, London, UK.
authors.forename: Raymond J
authors.initials: RJ
authors.lastname: Dolan
authors.affiliation: Department of Neuroscience, University of Arizona, Tucson, AZ 85721, USA.
authors.forename: Nicholas J
authors.identifier: http://orcid.org/0000-0002-1115-1774
authors.initials: NJ
authors.lastname: Strausfeld
authors.affiliation: Institute of Psychiatry, Psychology & Neuroscience, Department of Basic & Clinical Neuroscience, King's College London, London, UK frank.hirth@kcl.ac.uk.
authors.forename: Frank
authors.initials: F
authors.lastname: Hirth
mesh_terms: D000818:Animals; D001522:Behavior, Animal; D005075:Biological Evolution; D001921:Brain / Q000033:anatomy & histology / Q000502:physiology*; D004298:Dopamine; D056228:Feedback, Sensory; D007313:Insecta / Q000033:anatomy & histology* / Q000502:physiology; D009415:Nerve Net; D012098:Reproduction; D012679:Sense Organs; D014714:Vertebrates / Q000033:anatomy & histology* / Q000502:physiology
chemical_list: D004298:Dopamine
keywords: action selection; attractor state; basal ganglia; brain evolution; central complex; sensorimotor representation