Localization of a Short-Term Memory in Drosophila

Abstract

Memories are thought to be due to lasting synaptic modifications in the brain. The search for memory traces has relied predominantly on determining regions that are necessary for the process. However, a more informative approach is to define the smallest sufficient set of brain structures. The rutabaga adenylyl cyclase, an enzyme that is ubiquitously expressed in the Drosophila brain and that mediates synaptic plasticity, is needed exclusively in the Kenyon cells of the mushroom bodies for a component of olfactory short-term memory. This demonstrates that synaptic plasticity in a small brain region can be sufficient for memory formation.

Multiple Memory Traces for Olfactory Reward Learning inDrosophila

“…For all behavioral experiments, F1 progeny of the following crosses were measured: females of rut 2080 ; UAS-rut (III ) or wild-type Canton-S were mated to males of w; MB247 (III ), w; GH146 (II ), w; NP225 (II ), w; MB247 (III), (III ),w;GH146; (III ), or w 1118 (Zars et al, 2000;Heimbeck et al, 2001;McGuire et al, 2003). MB247, GH146, and NP225 are the GAL4 driver lines directing the expression in the KCs (MB247 ) and PNs (the other two).…”

“…To address the possibility of multiple traces in PNs and KCs for the short-term olfactory memory, we decided to map sufficient cell groups for rescuing the memory of rutabaga (rut) mutant with targeted expression of wild-type rut cDNA (Zars et al, 2000). The rut gene encodes a type I calcium/calmodulinactivated adenylate cyclase (AC) Levin et al, 1992) onto which the internally processed conditioned stimulus (CS; odor) and unconditioned stimulus (electroshock or sugar) are supposed to converge (Abrams et al, 1998).…”

“…In both olfactory shock learning and sugar reward learning, short-term memory of the rut mutant is reduced (Tempel et al, 1983;Tully and Quinn, 1985). Wild-type rut expression localized to the KCs rescues the aversive and appetitive olfactory memory of the mutant to the wild-type level (Zars et al, 2000;Schwaerzel et al, 2003), suggesting that these KCs can serve as a shared sufficient site for two differently reinforced memory traces. Taking the advantage of this experimental system, we addressed the ability of PNs to form the rut-dependent trace for rewarded and punished olfactory memories at different time points (up to 3 h).…”

Operant conditioning in invertebrates

“…Many of these genes affect the level of the second-messenger cAMP and are preferentially expressed in a prominent neuropil in the fly's brain, the mushroom bodies (Figure 1b; [12][13][14]). For some of these genes, being expressed exclusively in the mushroom bodies is sufficient for normal learning [15]. Are those genes also involved in operant conditioning?…”

“…The picture that emerges suggests that the mushroom bodies are needed for chemosensory learning and higher-order integrative tasks [23 ]. Although the cAMP cascade and its downstream targets are both necessary and sufficient in the mushroom bodies for these tasks [15,22], in operant conditioning they are involved in neurons outside the mushroom bodies and in a different way than in classical conditioning [19 ].…”