Cognition with few neurons: higher-order learning in insects

Insects possess miniature brains but exhibit a sophisticated behavioral repertoire. Recent studies have reported the existence of unsuspected cognitive capabilities in various insect species that go beyond the traditionally studied framework of simple associative learning. Here, I focus on capabilities such as attentional modulation and concept learning and discuss their mechanistic bases. I analyze whether these behaviors, which appear particularly complex, can be explained on the basis of elemental associative learning and specific neural circuitries or, by contrast, require an explanatory level that goes beyond simple associative links. In doing this, I highlight experimental challenges and suggest future directions for investigating the neurobiology of higher-order learning in insects, with the goal of uncovering the basic neural architectures underlying cognitive processing.

Introduction

Insects have historically fascinated biologists for the access they allow to the mechanisms and organization of behavior. The fact that insects possess miniature nervous systems, with a low number of neurons (e.g., 100 000 neurons in the fruit fly brain [1] or one million in the bee brain [2] versus 85 billion in the human brain [3]), does not constitute a limitation for the production of sophisticated and complex behaviors 4, 5, 6. Numerous insect species such as bees, ants, parasitoid wasps, fruit flies, moths, butterflies, hissing bugs, crickets, grasshopper, and locusts, learn and memorize different sorts of sensory cues as predictors of reward 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19 or punishment 20, 21, 22, 23, 24, 25, 26 and form memories of such experiences that can be retrieved at different times after learning, from the short- long-term range. The neural circuits underlying such capabilities are only simple in appearance but exhibit an exquisite architecture [27].

The past decade has generated a wealth of novel research on insect learning and memory that has overcome the classical framework of simple forms of associative learning to focus on more elaborate cognitive capabilities 4, 5. This includes work on attention-like processes in fruit flies and honey bees 28, 29, pessimistic biases [30], and concept learning in bees 31, 32, 33. These reports shed new light on the cognitive richness of insect behavior, which seems to transcend basic Pavlovian and operant learning. Yet, at the same time, they may tend to create a feeling of wonder in non-scientific members of the public, usually promoted by biased media reports or by scientists themselves, which revolves around a growing tendency of attributing too easily humanlike qualities to animals [34]. In the light of such an undesired effect, the critical question is not, therefore, whether insects achieve ‘marvelous feats’, but how they achieve them. Here, I focus on a selection of recent findings in insect cognitive behavior and analyze the neural mechanisms known to mediate such behavior. I discuss whether behaviors that appear particularly complex can be explained on the basis of elemental associative learning and specific neural circuits or, by contrast, require an explanatory level that goes beyond this level.