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What insects can tell us about the origins of consciousness

University of California

Australian Research Council
PNAS Direct Submission
National Academy of Sciences

Michael S. Gazzaniga
Bjorn Merker

von Holst
Tim Bayne
Lars Chittka
Jean-Marc Devaud
Stanley Heinze
Michael Gillings
Peter Godfrey-Smith
Marcus J. A. Plath




Santa Barbara

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The New York Times
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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. Therefore, we argue the insect brain also supports a capacity for subjective experience. 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. NCC results thus tend to be biased toward complex cortical structures and cannot generalize to animals lacking a cortex.In this review, we will suggest an alternative approach to studying the capacity for subjective experience in invertebrates. We therefore conclude that if subjective experience is indeed supported by midbrain structures in humans, then insects also have the capacity for a form of subjective experience.Finally, we propose that a capacity for subjective experience probably evolved early in the history of animal life for specific animal clades. Rather, the proposal is that subcortical structures support the basic capacity for experience, the detailed contents of which might be elaborated by or otherwise depend upon cortical structures (32).We will adopt and expand the account given by Merker (8), who argues that subjective experience arises from interacting midbrain and basal ganglia structures creating an integrated simulation of the state of the animal’s own mobile body within the environment.Merker suggests that an important function of the midbrain is to combine interoceptive (stimuli arising from within the body) and exteroceptive (stimuli external to the body) sensory information. Vertebrates organize their behavior by reference to this integrated model of the environment rather than by reacting to independent sensory inputs (8, 33).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. This arrangement allows a point of convergence for processed spatially structured information, in turn allowing an integrated sense of space that includes the position, state, and movement of the body (9, 40⇓–42).Organizing behavior by reference to an integrated simulation of the state of the mobile body in space also provides an efficient neural solution for resolving the confusing sensory input caused by self-motion [the so-called reafference problem (43)]. Integrative structures within the midbrain and basal ganglia, including the periaqueductal gray, substantia nigra, ventral thalamus, striatum, and midbrain reticular formation, combine this information on introspective assessment of state with exteroceptive assessment of location in space to collate and resolve competing motivations, prioritize resources, and select targets and actions (8, 33).Midbrain and basal ganglia structures thus provide an effective and efficient neural solution for decision making (Fig. 1A). Analyses and modeling of basal ganglia function in vertebrates have emphasized how drawing together all evidence for different possible actions within a unified neural system enables an effective and efficient solution for action selection, without having to posit a higher-level decision maker reflecting on the decision (57⇓–59).Placing the basic capacity for subjective experience in subcortical structures does not rule out a role for the cortex and other subcortical systems (including hippocampal systems) in conscious experience. The insect brain resolves action and target selection, processes sensory information, and clearly executes a command function over the behavioral system (72).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. 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.A compelling demonstration of the command function of the insect brain for the total behavioral system of the insect is the effect of focused injection of neurotransmitter agonists and antagonists to the region of the central complex (CX) of the insect brain. This example shows that the central brain structures are key for the initiation and direction of movement in cockroaches and crickets (74, 75).Further, the CX of the insect brain seems specialized for the processing of spatial information and organization of movement (76). The P is premotor, and emerging evidence suggests that competitive processing within structures of the P contributes to effective action selection based on all available sensory information (93⇓⇓–96).In sum, new functional analyses of the insect brain emphasize how it supports a behavioral core control system that is functionally analogous to that of the vertebrate midbrain (Fig. 2). There is now both behavioral and electrophysiological evidence that the neural modeling of the environment performed by insects involves multiple layers of filtering of sensory information to support selective attention to stimuli that are salient and suppression of representation of irrelevant stimuli (101⇓⇓–104). These exciting new electrophysiological studies demonstrate more compellingly than behavioral studies alone the subjective and egocentric nature of the neural representation of the environment in insects, and their capacity for selective attention supports our assertion that insects have a capacity for subjective experience. That is strong evidence that the insect brain has the capacity to support subjective experience.Our thesis raises two related questions. There are other, simpler ways to organize animal behavior than by creating the kind of integrated neural simulation seen in the insect and vertebrate core control systems. elegans can also support various forms of learning such as habituation (114⇓–116) and classical associative conditioning (116⇓–118), enabling adaptive change in behavior with experience.Nematodes are thus able to integrate multiple forms of sensory input using a centralized nervous system, but it seems that their behavior is organized as responses either to the immediate sensory environment or to immediate interoceptive signals of physiological state. In such environments, very simple behavioral control systems are sufficient.If the insect brain supports subjective experience, then this not only increases the diversity of animals considered to have these abilities—it also requires a reconsideration of when this ability might have appeared on Earth. It is plausible that some of the Cambrian fauna within both the basal vertebrate and arthropod groups had a capacity for subjective experience.It is presently unclear whether the insect and vertebrate behavioral core control systems evolved independently. If this interpretation is correct, it would imply that a brain with a form of higher sensory integration center may even predate the divergence of these groups.We have argued that insects possess a capacity for subjective experience.

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