What insects can tell us about the origins of consciousness

Abstract

How, why, and when consciousness evolved remain hotly debated topics. Addressing these issues requires considering the distribution of consciousness across the animal phylogenetic tree. Here we propose that at least one invertebrate clade, the insects, has a capacity for the most basic aspect of consciousness: subjective experience. In vertebrates the capacity for subjective experience is supported by integrated structures in the midbrain that create a neural simulation of the state of the mobile animal in space. This integrated and egocentric representation of the world from the animal's perspective is sufficient for subjective experience. Structures in the insect brain perform analogous functions. Therefore, we argue the insect brain also supports a capacity for subjective experience. In both vertebrates and insects this form of behavioral control system evolved as an efficient solution to basic problems of sensory reafference and true navigation. The brain structures that support subjective experience in vertebrates and insects are very different from each other, but in both cases they are basal to each clade. Hence we propose the origins of subjective experience can be traced to the Cambrian.

Keywords: central complex; primary consciousness; subjective experience; vertebrate midbrain.

Fig. 1.

Structures of the vertebrate midbrain (not to scale) supporting the behavioral “core control system.” The vertebrate midbrain supports an integrated multisensory model of the state of the animal in space, which supports effective decision making. (A) Decision making involves an assessment of what is needed and where and how the needed resources can be obtained. Decision making can therefore be considered to involve three domains: internal motivations, target selection, and action selection [adapted from the “selection triangle” proposed by Merker (8)]). These domains interact and can be resolved by referencing an integrated neural model that contains information on the state of self, self movement, environmental state and structure, and memory of prior experience. These elements of the neural model are supported by midbrain structures (B). As a simplification, regions are colored according to their primary function(s) in the neural model described in A. The superior colliculus [part of the tectum (TEC) forming the roof of the midbrain] receives topographically organized multisensory input and creates an integrated neural model of the organism moving in space (8). The floor of the midbrain is formed by the hypothalamic structures (Hyp) and associated nuclei [pituitary (pt) and mammillary bodies (M)] that collate information on the physiological status of the organism referenced with prior experience, to identify needs to maintain a homeostatic optimum (15, 56). Integrative structures within the midbrain and basal ganglia, including the periaqueductal gray (P), substantia nigra (N), thalamus (Tha), striatum (St), and midbrain reticular formation (MR), integrate these sources of information (8, 33) (A). In advanced vertebrates the cortex and hippocampal structures clearly have a very strong input in to this system, but this midbrain system is not dependent on cortical inputs to function (140) and is highly conserved across all vertebrate lineages (33).

Fig. 2.

Basic functional anatomy of the insect brain (not to scale). The structures of the insect brain create an integrated neural model of the state of the insect in space that is functionally analogous to that described for the vertebrate brain in Fig. 1. Regions are colored to reflect the major functions described in Fig. 1A. Vision and smell are primarily processed by dedicated sensory lobes, which function to refine and enhance sensory representations and enhance distinctions between similar stimuli (95, 141). Primary odor processing is performed in the antennal lobes (AL). Visual processing is performed by the lamina (LA), medulla (ME), and lobula (LO). The MB supports learning and memory (–146). The CX is anatomically variable between insect orders but typically is composed of the central body upper (CBU), central body lower (CBL), and noduli (NO). It has several specializations for processing spatial information corrected for self movement (75, 76, 83, 87). The protocerebrum (P) is an anatomically complicated region. Modulatory and inhibitory connections to and within the protocerebrum convey information on physiological state (94, 95), and structures within the protocerebrum, particularly the lateral accessory lobe, are involved in integration of information, hence the hatched shading.