Glutamatergic activity in the amygdala signals visceral input during taste memory formation

Abstract

Conditioned taste aversion (CTA) is a learning paradigm in which an animal avoids a taste (conditioned stimulus) previously associated with visceral toxic effects [or unconditioned stimulus (US)]. Although many studies have implicated glutamate-mediated neurotransmission in memory consolidation of different types of learning tasks, including CTA, the exact role of this neurotransmitter system in memory formation is not known. Thus, we set out to determine whether glutamate mediates signaling of the US in CTA. We present evidence obtained by in vivo microdialysis that the US (i.p. injection of lithium chloride) induced a dramatic increase in glutamate release in the amygdala and a modest but significant release in the insular cortex. Moreover, CTA can be elicited by intra-amygdalar microinjections of glutamate; consequently, when glutamate is administered just before the presentation of a weak US, a clear CTA is induced. In contrast, the injection of glutamate alone or glutamate 2 h after the suboptimal US did not have any effect on the acquisition of CTA. These results indicate that glutamate activation of the amygdala can partially substitute the US in CTA, thus providing a clear indication that the amygdala conveys visceral information for this kind of memory.A number of studies (1-5) have implicated glutamatemediated transmission in consolidation of memory for different types of training, such as inhibitory avoidance, Morris water maze, and conditioned taste aversion (CTA). CTA is a learning paradigm in which the novel taste of food or drink (conditioned stimulus, CS) is paired with visceral signals of poisoning (unconditioned stimulus, US). Consequently, the animals avoid consuming the food or drink previously associated with toxic effects. CTA has unique properties; it is established after a single trial, permits long delays between stimuli presentation, and lasts for very long periods of time, even weeks. This feature makes it possible to separate the acquisition process into phases-CS presentation and US presentation-which can be studied independently under different experimental treatments (6).CTA is established by the interaction of brainstem, limbic, and neocortical structures underlying different phases of the acquisition storage and retrieval of gustatory memory (7). Among the structures involved in the initial phases of taste memory formation are the gustatory neocortex and amygdala (8). Thus, damage to either the gustatory insular cortex (IC) or amygdala in adult rats leads to impaired acquisition of CTA (6,7,[9][10][11][12][13][14][15][16][17]. However, the functional roles of IC and amygdala seem to be different during the phases of taste memory formation. Functional blockade of IC before taste presentation, but not between taste presentation and lithium chloride (LiCl) injection, blocks CTA (16, 18), suggesting that the gustatory cortex is involved in taste processing and͞or memory but is not necessary for processing the visceral signals of poisoning. Conversely, amygdala functional inactivation...

Learning-Related Plasticity of Temporal Coding in Simultaneously Recorded Amygdala–Cortical Ensembles

“…Furthermore, when tetanic stimulation is applied to BLA [a procedure that induces NMDA-dependent long-term potentiation in GC (Jones et al, 1999;Escobar et al, 1998aEscobar et al, ,b, 2002] immediately before CTA induction, retention of the learning is enhanced (Escobar and Bermudez-Rattoni, 2000). A weak CTA can be enhanced by intra-BLA infusion of glutamate (Miranda et al, 2002), but this effect is blocked by NMDA receptor blockade in GC (Ferreira et al, 2005), again suggesting that amygdalocortical connections are an important part of CTA learning. Relatedly, a recent report (Bauer et al, 2007) shows that ␥-oscillatory (35-45 Hz) field potential coherence between BLA and rhinal cortex increases across 6 d of learning to respond to a visual cue paired with a food reward.…”

“…Palatability-related information only appears in GC between 0.8 and 1.0 s after taste administration (Katz et al, 2001a); CTA, which changes taste palatability without affecting actual taste quality (Berridge and Robinson, 1998), would therefore be predicted to change only these later aspects of GC taste responses . Indirect evidence, meanwhile, suggests that activity in BLA, which is known to code palatability (Nishijo et al, 1998), may drive CTA-related activity and plasticity in GC (Escobar et al, 1998a,b;Escobar and Bermudez-Rattoni, 2000;Miranda et al, 2002;Ferreira et al, 2005). Thus, learning should change earlier aspects of BLA responses than GC responses [i.e., learning should change BLA responses produced Ͻ1 s after stimulus administration; for similar logic in fear conditioning, see Quirk et al (1997), Armony et al (1998), and Repa et al, 2001].…”

Internal body state influences topographical plasticity of sensory representations in the rat gustatory cortex

“…10. The association between CS and US is likely to happen at the brainstem level, in the parabrachial nucleus, the US-relevant (visceral) information is transmitted to the amygdala and then to the cortex via glutamatergic projections (30), whereas taste-related information follows a classical brainstemthalamic pathway (31). The role of the insular cortex (containing primary GC) in CTA has been the topic of several studies (12,21).…”

Behavioral tagging is a general mechanism of long-term memory formation

“…Saccharin consumption (in percentage) was calculated as consumption test ϫ 100/consumption acquisition. For the induction of a strong CTA-LTM, the LiCl solution used was 0.4 M (7.5 mL/kg) (37).…”