Genetic Distortion of the Balance between Punishment and Relief Learning inDrosophila

Abstract

An experience with electric shock can support two opposing kinds of behavioral effects: Stimuli that precede shock during training are subsequently avoided as predictors for punishment, whereas stimuli that follow shock during training are later on approached, as they predict relief. We show here, for the fruit fly Drosophila, that upon the loss of white-function, the balance between these two kinds of learning is distorted in favor of punishment learning: white 1118 mutants show stronger punishment learning and weaker relief learning, as compared to wild type flies. Thus, white 1118 mutants establish, overall, more ''negative'' memories for the shock experience. This only concerns the mnemonic effects of the shock; the immediate, reflexive responsiveness to shock remains unaltered. Also, learning about reward is apparently unaffected, both in adult and larval Drosophila. Prompted by the proposed function of the White protein as the transporter for biogenic amine precursors, we probed the brains of white 1118 mutants for the amounts of biogenic amines (octopamine, tyramine, dopamine, and serotonin) by using high-pressure liquid chromatography coupled to mass spectrometry. Using this method, we found, however, no difference between white 1118 and wild type flies for any of the probed amines. In any event, analyses of how the white 1118 mutation affects the balance between punishment and relief learning should provide a study case of how heritable distortions of such balance can come about. Finally, the effects of the white 1118 mutation should be considered as a source of confound when using white-as the ''marker gene'' in behavior-genetic analyses of any sort.

Behavioral and Synaptic Plasticity Are Impaired upon Lack of the Synaptic Protein SAP47

“…5AЈ) (onesample sign tests: p Ͻ 0.05/2; N ϭ 16, 16) at equal levels ( Fig. 5AЈ) ( p ϭ 0.66, U ϭ 109; sample sizes as above) (see also Yarali et al, 2009). Therefore, data obtained with transgenic strains in our paradigm can be interpreted without reference to white function.…”

“…Therefore, genetic controls were established by crossing the respective transgenic strains to a w 1118 strain (in the case of the RNAi experiment) or a w 1118 ; Sap47 156 strain (in the case of the rescue experiments). To see whether the w 1118 mutation may have an effect, either on associative learning (Diegelmann et al, 2006;Yarali et al, 2009) or on SAP47 expression, we compared w 1118 with WT larvae in odorant-reward associative ability as well as by Western blot analysis (see Fig. 5 A, AЈ).…”

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

“…In two further studies, the neurogenetic bases of fly relief-learning were investigated: First, the role of the white gene (CG2759) in relief-learning was tested (Yarali et al 2009b). The white gene product forms one-half of an ATP-binding transmembrane transporter (O'Hare et al 1984).…”

“…1) (we use "relief" to refer specifically to the acute effects of punishment offset; an equally legitimate yet broader use of the word in, e.g., "fear relief," encompasses any process that eases fear [Riebe et al 2012]). Indeed, in experimental settings, it turns out that stimuli experienced before and during a punishing episode are later avoided as they signal upcoming punishment, whereas stimuli experienced after a painful episode can subsequently prompt approach behavior, arguably (Box 1) because of their association with the relieving cessation of pain (Konorski 1948;Smith and Buchanan 1954;Wolpe and Lazarus 1966;Zanna et al 1970;Solomon and Corbit 1974;Schull 1979;Solomon 1980;Wagner 1981;Walasek et al 1995;Tanimoto et al 2004;Yarali et al 2008Yarali et al , 2009bAndreatta et al 2010Andreatta et al , 2012Yarali and Gerber 2010;Ilango et al 2012;Navratilova et al 2012;Diegelmann et al 2013b); for a corresponding finding in the appetitive domain, see Hellstern et al (1998) and Felsenberg et al (2013). Such relief can both support the learning of the cues associated with the disappearance of the threat and reinforce those behaviors that helped to escape it.…”

Inter-leg coordination in the control of walking speed inDrosophila

“…It is important to note that these low octopamine levels might only explain reduced walking speed in w 1118 , Tbh nM18 . While w 1118 also has reduced levels of other biogenic amines like dopamine and serotonin (Sitaraman et al, 2008), its octopamine levels are similar to wild-type or are only very slightly reduced (Sitaraman et al, 2008;Yarali et al, 2009). Modifying octopamine levels might be useful in future studies in order to specifically modulate the walking behavior in Drosophila mainly with regard to movement speed.…”