Differential Associative Training Enhances Olfactory Acuity inDrosophila melanogaster

Abstract

Training can improve the ability to discriminate between similar, confusable stimuli, including odors. One possibility of enhancing behaviorally expressed discrimination (i.e., sensory acuity) relies on differential associative learning, during which animals are forced to detect the differences between similar stimuli. Drosophila represents a key model organism for analyzing neuronal mechanisms underlying both odor processing and olfactory learning. However, the ability of flies to enhance fine discrimination between similar odors through differential associative learning has not been analyzed in detail. We performed associative conditioning experiments using chemically similar odorants that we show to evoke overlapping neuronal activity in the fly's antennal lobes and highly correlated activity in mushroom body lobes. We compared the animals' performance in discriminating between these odors after subjecting them to one of two types of training: either absolute conditioning, in which only one odor is reinforced, or differential conditioning, in which one odor is reinforced and a second odor is explicitly not reinforced. First, we show that differential conditioning decreases behavioral generalization of similar odorants in a choice situation. Second, we demonstrate that this learned enhancement in olfactory acuity relies on both conditioned excitation and conditioned inhibition. Third, inhibitory local interneurons in the antennal lobes are shown to be required for behavioral fine discrimination between the two similar odors. Fourth, differential, but not absolute, training causes decorrelation of odor representations in the mushroom body. In conclusion, differential training with similar odors ultimately induces a behaviorally expressed contrast enhancement between the two similar stimuli that facilitates fine discrimination.

Aversive olfactory associative memory loses odor specificity over time

“…Thus 24 h after training, learned avoidance was not specific to the trained odor at all; instead, it was fully generalized to a novel odor. Using two other odors, 3-octanol and 1-octen-3-ol, with partially overlapping neural representations (Campbell et al, 2013; Barth et al, 2014), we corroborated the partial specificity of learned avoidance at 20 min after training, and the lack of specificity after 24 h (Fig. 1C).…”

“…(i) Learned avoidance after associative odor–electric shock training lost its specificity for the trained odor with the passage of time, as previously shown for odor–food reward memory in adult flies (Ichinose et al, 2015). (ii) The specificity of long-term learned avoidance was enhanced when training and testing explicitly promoted and required discrimination between two odors, paralleling the situation with respect to short-term aversive and appetitive memories in adult and larval Drosophila , respectively (Barth et al, 2014; Mishra et al, 2010). (iii) Other parameters of training, i.e.…”

Pain-relief learning in flies, rats, and man: basic research and applied perspectives

“…Interestingly, in accord with prediction-error signaling (Rescorla 1988), punishment-trained odors not only enable conditioned behavior but also apparently induce feedback onto dopaminergic neurons (Riemensperger et al 2005; see the seminal study of Hammer 1993 for a corresponding finding in honeybee appetitive learning). Other, nontrained odors support conditioned avoidance only to the extent that they are similar in quality (Niewalda et al 2011;Campbell et al 2013;Barth et al 2014) and/or intensity (Yarali et al 2009a) to the actually trained odor. Appetitive learning, using sugar as reward is, in principle, organized in a similar way (e.g., Schwaerzel et al 2003;Keene et al 2006;Trannoy et al 2011), with at least two significant differences: † It has been argued that, in addition to the Kenyon cells, there may be an odor-reward short-term memory trace in the projection neurons (Drosophila, Thum et al 2007;honeybee, Menzel 2001;Giurfa and Sandoz 2012;Menzel 2012; but see Peele et al 2006).…”

“…In any event, the STDP-based model by Drew and Abbott (2006) does not predict safety-learning as a result of unpaired presentations of odor and shock. Such unpaired-training can, however, have mnemonic consequences: In larval Drosophila unpaired presentations of odor and a sugar reward turn the odor into a predictor of no-reward Barth et al 2014; concerning honeybees, see Hellstern et al 1998 and references therein). Also, given the innate Yarali et al (2008).…”

Odor-Induced Multi-Level Inhibitory Maps inDrosophila

“…Mice show accelerated discrimination ability when synaptic inhibition of mitral cells is increased by selectively altering granule cell function (Abraham et al, 2010). In locusts and flies, disruptive manipulation of the GABAergic AL network reduces the insects' ability to behaviorally discriminate between similar odors (Stopfer et al, 1997;Barth et al, 2014). The similarity between glomerular excitation patterns evoked by different odors often matches with the animals' ability to discriminate between the odors in behavioral tasks (Sachse and Galizia, 2003;Guerrieri et al, 2005;Niewalda et al, 2011;Barth et al, 2014;Carcaud et al, 2018).…”