Configural Olfactory Learning in Honeybees: Negative and Positive Patterning Discrimination

Abstract

In an appetitive context, honeybees (Apis mellifera) learn to associate odors with a reward of sucrose solution. If an odor is presented immediately before the sucrose, an elemental association is formed that enables the odor to release the proboscis extension response (PER). Olfactory conditioning of PER was used to study whether, beyond elemental associations, honeybees are able to process configural associations. Bees were trained in a positive and anegative patterning discrimination problem. In the first problem, single odorants were nonreinforced whereas the compound was reinforced. In the second problem, single odorants were reinforced whereas the compound was nonreinforced. We studied whether bees can solve these problems and whether the ratio between the number of presentations of the reinforced stimuli and the number of presentations of the nonreinforced stimuli affects discrimination. Honeybees differentiated reinforced and nonreinforced stimuli in positive and negative patterning discriminations. They thus can process configural associations. The variation of the ratio of reinforced to nonreinforced stimuli modulated the amount of differentiation. The assignment of singular codes to complex odor blends could be implemented at the neural level: When bees are stimulated with odor mixtures, the activation patterns evoked at the primary olfactory neuropile, the antennal lobe, may be combinations of the single odorant responses that are not necessarily fully additive.

Biological constraints on configural odour mixture perception

“…Negative patterning, a special type of differential conditioning task, involves discriminating between a binary mixture and each of its components. In this procedure, two odorants are rewarded when presented alone (X+, Y+) but not when presented in a mixture (XY-; Deisig et al, 2001). Negative patterning is a difficult task for bees and only a small proportion manage to differentiate the stimuli at the end of training (Deisig et al, 2001(Deisig et al, , 2002(Deisig et al, , 2003Komischke et al, 2005;Devaud et al, 2015).…”

“…In this procedure, two odorants are rewarded when presented alone (X+, Y+) but not when presented in a mixture (XY-; Deisig et al, 2001). Negative patterning is a difficult task for bees and only a small proportion manage to differentiate the stimuli at the end of training (Deisig et al, 2001(Deisig et al, , 2002(Deisig et al, , 2003Komischke et al, 2005;Devaud et al, 2015). Indeed, each element (X or Y) is presented as often with the sucrose reward as without, so configural processing of the mixture is necessary to solve this task (Deisig et al, 2001;Devaud et al, 2015).…”

“…Negative patterning is a difficult task for bees and only a small proportion manage to differentiate the stimuli at the end of training (Deisig et al, 2001(Deisig et al, , 2002(Deisig et al, , 2003Komischke et al, 2005;Devaud et al, 2015). Indeed, each element (X or Y) is presented as often with the sucrose reward as without, so configural processing of the mixture is necessary to solve this task (Deisig et al, 2001;Devaud et al, 2015). Recently, bees' negative patterning performances were compared between AB (91/9the ratio was adapted so that bees detected the two components equally well) and a list of control mixtures (Wycke et al, 2020).…”

Smell and Aftersmell: Fast Calcium Imaging Dynamics of Honey Bee Olfactory Coding

“…Conversely, when the reward precedes the stimulus (backward conditioning), no positive association can be established (Felsenberg et al, 2014; Hellstern et al, 1998) . It also enables the study of more sophisticated cognitive processes such as trace learning (Paoli et al, 2023a; Szyszka et al, 2011) and patterning discrimination (Deisig et al, 2001; Devaud et al, 2015) . In the former, CS and US are not overlapping but separated by a stimulus-free temporal gap, whereas in the latter, bees are trained to respond in opposite ways to a two-odorant mixture compared to its individual components (Deisig et al, 2001; Devaud et al, 2015) .…”

Assessing complex odor discrimination in mice using a novel instrumental patterning task.

“…Such mechanisms of stimulus representation are typically studied using go/no-go negative patterning tasks. In these tasks, individual stimuli are reinforced (Aþ/Bþ), but their compound presentation is not (ABÀ; Deisig et al, 2001;Harris et al, 2008;Myers et al, 2001;Redhead & Pearce, 1995;Rescorla, 1972Rescorla, , 1973. The discrimination between Aþ/Bþ and ABÀ stimuli cannot be explained by the accrual of associative strength of the former.…”