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.

Keywords: action selection; attractor state; basal ganglia; brain evolution; central complex; sensorimotor representation.

Figure 1.

Principal arrangements of the insect central complex, the lamprey and primate basal ganglia and their associated loops. (a) (i) Simplified schematic of the central complex (CX) showing connections between the protocerebral bridge (PB), fan-shaped body (FB) and ellipsoid body (EB), along with two satellite neuropils, the Gall and lateral accessory lobe (LAL). The noduli have been omitted. The PB is divided into synaptic modules which, depending on the species, vary between symmetrical arrangements of 9 + 9 (in Drosophila, Mantis religiosa) and as few as 5 + 5 (Notonecta) units. PB modules encode sensory representations (visual/tactile) from eight sectors on each side of the animal's long axis. Left and right representations of this ‘where’ code are relayed across eight modules of the FB such that left and right maps from the PB are compared. Outputs from the FB project into 16 modules of the EB such that modules representing opposite sectors are adjacent. The PB receives numerous inputs, including neurons entering laterally (arrows) carrying high-level information about visual motion direction. Columnar module in the FB are intersect by many dendritic trees and terminals (two shown) that likewise carry synthesized sensory information about complex parameters (‘what’ inputs) as well as a broad palette of modulatory peptides. The EB also receives a variety of inputs (also ‘what’ afferents), such as from the Gall and other satellite neuropils. Different combinations of where and what inputs result in different levels of activity in EB modules. Competing strengths of activity among EB modules result in a few achieving a stable output to the LAL. Further connections link the LAL system to pre-motor descending neurons (not shown). (ii) Comparison between sensorimotor and associative loops in insects (using the anatomy of the Drosophila as a general model) and sensorimotor, associative and ventral loops in mammals (using primates and humans in particular as a general model). Spatial organization is highlighted by the presence of numerically ordered modules in PB, FB, EB and LAL. The grey and bold black fonts indicate modules on the left and right side, respectively. (b) Anatomical representation of the re-entrant neural circuits characterizing sensorimotor and associative selections in the lamprey, which diverged already 560 Ma from the vertebrate lineages. (i) The first re-entrant neural circuit involves BG, thalamus and areas such as the optic tectum or the MLR, which provide sensorimotor inputs to the striatum via thalamus and receive direct inhibitory output from the BG. (ii) The circuit involves BG, thalamus and pallium, which projects directly towards the striatum and in turn receives mediated (via thalamus) inhibitory output from the BG. (c) Sensorimotor, associative and ventral (limbic) loops in mammals, here shown for primates. In the left hemisphere in humans, the different colours highlight the connectivity between separate areas in the cortex and their specific targets in the striatum and thalamus. This parallel partial segregation is maintained throughout the basal ganglia in the GP (globus pallidus), STN and SNr. Abbreviations: PB, protocerebral bridge; FB, fan shape body; EB, ellipsoid body; LAL, lateral accessory lobes; Pal, pallium; Str, striatum; MLR, mesencephalic locomotor region; Thal, thalamus; GPe, globus pallidus external segment, GPi, globus pallidus internal segment; STN, subthalamic nucleus, SNr, substantia nigra pars reticulata; Cau, caudate; NAcc, nucleus accumbens; Put, putamen.

Figure 2.

Energy landscape illustrating nonlinear dynamics of a hypothetical neural network. The nonlinear dynamics of neural networks can be described in energy landscapes, where any starting condition of the system will cause the network to evolve and change its activity towards the closest low energy state, the ‘attractor’. (a) In this first example, two different starting conditions (A and B), initially located in a high energy position, reach the bottom of the basin offered by a single vast attractor state. The initial considerable differences in the input are ignored by the system which, via state transitions, reach the same stable point. (b) In this second example, the same starting conditions (A and B) in a similar high energy starting position are characterized by very different state transitions. State transition for A results in reaching the closest low energy state of a small attractor state, if compared with the attractor represented in (a). Conversely, state transition for B causes movement towards a very shallow area, where minor perturbation (e.g. by noise) can result in reaching any of three different unstable points and further perturbation can trigger frequent switch among these weak attractors. The same illustrative heat maps of the energy landscapes of an arbitrary network are depicted twice using different perspectives to highlight its three-dimensional features.

Figure 3.

Comparison of action selection circuitries in the insect central complex and vertebrate basal ganglia. Schematic representation of sensorimotor loop, underlying action selection in the (a) insect central complex and (b) vertebrate basal ganglia, together with modulatory dopaminergic loop. In both insects and vertebrates, the sensorimotor loop is responsible for processing multiple sensory stimuli that are somatotopically organized. Information about the selections performed is projected backwards via feedback excitatory parallel connections. The loop enables the creation of attractor states, which in turn result in noise cancellation, the detection and selection of the most salient stimulus (winner-take-all functionality) and rapid switching among attractor states thereby adapting to changes in the environment. The dopamine loop, via differential dopamine release, modulates gain of the sensorimotor loop, which in turn amplifies or suppresses the information entering the EB in insects and the BG in vertebrates. The dopaminergic loop is responsible for long-term memory formation (via reinforcement learning) and dynamic alteration of attractor states resulting via maintenance of sensory-driven flexibility (short-term memory). The internal wiring of CX and BG only allows a partial comparison as the information in insects is as yet incomplete. In particular, (*) directionality and the presence of parallel connectivity within the EB is a likely explanation of recent behavioural data, but the exact composition of these plausible internal pathways is not yet known. (**) The Gall, connected between PB, EB and LAL, projects towards the EB, but the specific targets in terms of EB layers have to be defined (e.g. the Gall might project towards the output layers only, as for STN in vertebrates). Finally, (***) the gating function performed by the EB may be realized via either parallel or centre-off inhibitory connections: the presence of a directionality in the EB strongly suggests the presence of parallel gating as it would match the computational requirements for the system. Abbreviations: PB, protocerebral bridge; FB, fan shape body; EB, ellipsoid body; interm. layers, intermediate layers; LAL, lateral accessory lobes; MLR, mesencephalic locomotor region; DLR, diencephalic locomotor region; GPe, globus pallidus external segment, GPi, globus pallidus internal segment; STN, subthalamic nucleus, SNr, substantia nigra pars reticulata.