Conceptual learning by miniature brains

Abstract

Concepts act as a cornerstone of human cognition. Humans and non-human primates learn conceptual relationships such as 'same', 'different', 'larger than', 'better than', among others. In all cases, the relationships have to be encoded by the brain independently of the physical nature of objects linked by the relation. Consequently, concepts are associated with high levels of cognitive sophistication and are not expected in an insect brain. Yet, various works have shown that the miniature brain of honeybees rapidly learns conceptual relationships involving visual stimuli. Concepts such as 'same', 'different', 'above/below of' or 'left/right are well mastered by bees. We review here evidence about concept learning in honeybees and discuss both its potential adaptive advantage and its possible neural substrates. The results reviewed here challenge the traditional view attributing supremacy to larger brains when it comes to the elaboration of concepts and have wide implications for understanding how brains can form conceptual relations.

Keywords: Apis mellifera; concept learning; honeybee; insect cognition; visual cognition.

Figure 1.

An individually marked free-flying bee collecting sucrose solution on a concentric-disc pattern.

Figure 2.

Sameness learning in honeybees [9]. (a) Y-maze used to train bees in a delayed matching-to-sample task. Bees entered into the maze to collect sugar solution on one of the back walls of the maze. A sample was shown at the entrance before bees accessed the arms of the maze. (b) Training protocol. A group of bees were trained during 60 trials with black-and-white, vertical and horizontal gratings (pattern group); another group was trained with colours, blue and yellow (colour group). After training, both groups were subjected to a transfer test with novel stimuli (patterns for bees trained with colours, colours for bees trained with patterns). (c) Performance of the pattern and the colour group in the transfer tests. Both groups chose the novel stimulus corresponding to the sample although they had no experience with such test stimuli.

Figure 3.

Above/below learning in honeybees [8]. (a) Training protocol. A group of bees were trained during 50 trials to fly into a Y-maze to choose black patterns on a white background. Patterns were a variable target disposed above/below a constant referent. Half of the bees were rewarded on the ‘target above referent’ relation whereas the other half was rewarded on the ‘target below referent’ relation. The referent was either the disc or the cross, depending on the group of bees trained. In the example shown, the referent is the cross and the relationship rewarded during training, indicated in pink, is ‘above’ (‘above the cross’). After training, three types of transfer tests were performed. (b) Performance in the transfer tests. ‘Correct choices’ indicate here choice of the previously rewarded relationship (‘above the cross’). Bees learned the concept of ‘above/below’ and transferred it to novel stimuli fulfilling the learned relationship (transfer test 1). Transfer tests 2 and 3 showed that neither the spatial location of the referent on the background nor the centre of gravity of stimuli was used as a discrimination cue to resolve the task.

Figure 4.

Simultaneous mastering of two concepts in honeybees [7]. Bees learned to use two concepts simultaneously: ‘above/below’ (or right/left) and ‘difference’. (a) Bees were trained with sucrose reward in a Y-maze to choose the stimulus presenting two different patterns (group 1) or two different coloured discs (group 2) in an above/below (or right/left) relationship depending on the group of bees. Appearances and relative position of the patterns varied from trial to trial. (b) After 30 training trials, four transfer tests were performed. In transfer test 1, ‘correct choices’ indicate choice of the previously rewarded spatial relationship; in transfer tests 2 and 3 and 4, the term indicates choice of the stimulus with 2 different images. In transfer test 1, bees transferred their choice to unknown stimuli presenting the appropriate spatial relationship despite belonging to a different modality. Transfer tests 2–4 demonstrated that bees also learned that the stimuli had to present two different images. Bees used both rules simultaneously.

Figure 5.

(a) Three-dimensional reconstruction of a honeybee brain. The mushroom bodies (MBs) are shown in red. (b) Three-dimensional reconstruction of a honeybee MB in frontal view (vmb) (kindly provided by R. Menzel, Free University of Berlin). Two calyces a lateral (l) and a medial one (m), fuse in a single peduncle (Pe). The somata of the Kenyon cells (KCs), which integrate the MB are located in the calyx bowl. The dendrites of the KC form the calyx which is subdivided in three main regions; the lip, the collar (col) and the basal ring (br). The axons of the KC subdivide and form the α or vertical lobe (vl), the β or medial lobe, and the γ layer (not shown). (c) Multi-modal representation in the MB calyces (kindly provided by Wulfila Gronenberg, University of Arizona). Top: the brain of a honeybee worker Apis mellifera; middle: the brain of a carpenter ant worker Camponotus floridanus; bottom: the brain of a male reproductive C. floridanus. Male ants do not forage and have MBs that are approximately half the size of those of a worker ant. The visual regions medulla (me) and lobula (lo) are shown in red and blue, respectively. The primary olfactory neuropiles, the antennal lobes (al), are shown in yellow; cb, central body; asot, anterior–superior optic tract; aiot, anterior–inferior optic tract; ca, calyces; ml, medial lobe. For each brain, a detail of the sensory afferences at the level of the calyces is shown using the yellow (antennal lobe), red (medulla) and blue (lobula) colour code. Kc1 are the ‘normal’ (‘spiny’) Kenyon cells that give rise to the vertical and medial lobes; Kc2 are the ‘clawed’ Kenyon cells that give rise to a γ layer in the MB lobes.