Scientific Understanding of Consciousness
Basal Ganglia Homology with Arthropod Central Complex
Science 12 April 2013: Vol. 340 no. 6129 pp. 157-161
Deep Homology of Arthropod Central Complex and Vertebrate Basal Ganglia
Nicholas J Strausfeld, Frank Hirth
1Department of Neuroscience, School of Mind, Brain and Behavior, University of Arizona, Tucson, AZ 85721, USA.
2MRC Centre for Neurodegeneration Research, Department of Neuroscience, Institute of Psychiatry, King’s College London, London SE5 8AF, UK.
The arthropod central complex and vertebrate basal ganglia derive from embryonic basal forebrain lineages that are specified by an evolutionarily conserved genetic program leading to interconnected neuropils and nuclei that populate the midline of the forebrain-midbrain boundary region. In the substructures of both the central complex and basal ganglia, network connectivity and neuronal activity mediate control mechanisms in which inhibitory (GABAergic) and modulatory (dopaminergic) circuits facilitate the regulation and release of adaptive behaviors. Both basal ganglia and central complex dysfunction result in behavioral defects including motor abnormalities, impaired memory formation, attention deficits, affective disorders, and sleep disturbances. The observed multitude of similarities suggests deep homology of arthropod central complex and vertebrate basal ganglia circuitries underlying the selection and maintenance of behavioral actions.
Vertebrate basal ganglia are evolutionarily conserved interconnected nuclei traceable to stem group taxa. Their ground pattern comprises four principal volumes: the striatum, the internal and external domains of the globus pallidus, the subthalamic nucleus, and the substantia nigra. Basal ganglia play a key role in selecting and maintaining adaptive behavior by conveying sensorimotor, limbic, and associative information corresponding to action selection among behavioral modules that are competing for the control of a limited set of motor programs. Focal lesions and dysfunction of the basal ganglia are associated with movement disorders, such as parkinsonism, dystonia, and abulia, as well as neuropsychiatric disorders, essentially affecting goal-directed behavior and habitual control.
Similar behavioral manifestations have been attributed to the arthropod central complex, which in insects and crustaceans comprises three interconnected midline centers: the protocerebral bridge, fan-shaped body, and ellipsoid body leading to the paired lateral accessory lobes. Central complexes can be traced to related arthropods, including Onychophora, and to Lophotrochozoa represented by polychaete annelids. Here, we review multiple lines of evidence suggesting deep homology of the vertebrate basal ganglia and the arthropod central complex in the selection and maintenance of adaptive behavior.
Similarities of brain structure, function, and behavior have been ascribed to convergent evolution. However, microRNA and ribosomal RNA data support a common origin of arthropods and vertebrates—a conjecture further corroborated by recent morphological and molecular evidence suggesting that Cnidaria represent a true outgroup to Bilateria. Monophyly of Bilateria, together with the presence of a midline neuropil in both annelids and arthropods, suggests that a central complex–like midline structure already existed in the common bilaterian ancestor before the split to Protostomia and Deuterostomia, which likely possessed a complex, tripartite brain. It follows that genealogical correspondence due to common evolutionary origin is the most parsimonious explanation for the observed multitude of similarities between basal ganglia and the central complex, which suggests that homologous circuits mediate comparable behavioral functions across phyla.
There is no a priori reason for rejecting the notion that the selection of an appropriate motor program by a brain is a plesiomorphic trait and that this trait, which is common across phyla, is provided by homologous circuits. Adaptive behaviors, selected by the CNS as responses to one or another environmental challenge, are universal phenotypes of organisms equipped with rostral brains that integrate bilateral sensory input for coordinated behavioral output. The likelihood that such a relationship was present in the ancestor of protostomes and deuterostomes is suggested by trace fossils from the end-Vendian and early Cambrian, which show that organisms accomplished bouts of elaborate searching strategies—that is, complex actions that were switched on and off.
The multitude of commonalities reviewed here suggests deep homology of the arthropod central complex and vertebrate basal ganglia. They indicate that the ancestral bilaterian brain already possessed clusters of midline-associated, interconnected basal forebrain neurons mediating the selection and maintenance of behavioral actions. Together with recent evidence for a common origin of higher brain centers involved in allocentric memory in worms and mice, these data suggest that the ground pattern of circuits essential for behavioral choice originated very early and have been maintained across phyla throughout evolutionary time.
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