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.

In vivo expansion of functionally integrated GABA ergic interneurons by targeted increase in neural progenitors

“…Finally, to gain insights into the behavioral impact of integrated supernumerary R neurons, we analyzed the motor behavior of lineage‐expanded flies. Ellipsoid body R neurons have been implicated in goal‐directed behavior, higher motor control, spatial orientation learning and memory, as well as in attention, arousal, and decision‐making, suggesting that R neurons are involved in the assessment of sensory information for adaptive behavior (Strausfeld & Hirth, ; Fiore et al , ). Indeed, previous studies showed that R neuron dysfunction affects sensory‐motor transformation and higher motor control (Fiore et al , ; preprint: Kottler et al ).…”

Prominent Inhibitory Projections Guide Sensorimotor Computation: An Invertebrate Perspective

“…Simplified circuit maps for four nonmammalian model organisms where sensorimotor transformations are experimentally well studied. [100][101][102][103][104][105][106][107] Here, a combination of seeded sensorimotor loops and inhibition as well as compartmentalization enable the fly to integrate multiple senses in the CX and respond accordingly. [1,6,97] Inhibitory neurons are key in integrating information from the hair cells and photoreceptors to drive movement via cilia and tentacles.…”

Building a functional connectome of the Drosophila central complex

“…While it is possible that our selection of Gal4 lines was unintentionally biased against output neurons, or that our technique otherwise missed a number of output pathways, the picture of the central complex that emerges is of a densely recurrent sensorimotor hub with relatively low dimensional output (much as proposed by some models e.g. Stone et al 2017;Fiore et al 2015;Strauss and Berg 2010). The implications of this bottleneck for motor control remains a challenge for future studies to resolve.…”