Temporary basolateral amygdala lesions disrupt acquisition of socially transmitted food preferences in rats

Abstract

Lesions of the basolateral amygdala (BLA) have long been associated with abnormalities of taste-related behaviors and with failure in a variety of taste-and odor-related learning paradigms, including taste-potentiated odor aversion, conditioned taste preference, and conditioned taste aversion. Still, the general role of the amygdala in chemosensory learning remains somewhat controversial. In particular, it has been suggested that the amygdala may not be involved in a form of chemosensory learning that has recently received a substantial amount of study-socially transmitted food preference (STFP). Here, we provide evidence for this involvement by pharmacologically inactivating the basolateral amygdala bilaterally during STFP training. The same inactivation sites that impaired taste aversion learning eliminated the normally conditioned preference for a food smelled on a conspecific's breath. Impairments of learned preference persisted even in testing sessions in which BLA was not inactivated, and learning was normal when the BLA was inactivated only during testing sessions; thus, the impairment was a true acquisition deficit. In conjunction with previous results from other paradigms, therefore, our data suggest that the amygdala is vital for learning procedures involving pairings of potent and arbitrary chemosensory stimuli.In rodents, the amygdala is one of the major recipients of gustatory and olfactory information. The basolateral amygdala (BLA) receives olfactory projections from the olfactory piriform cortex and gustatory projections from the parabrachial nuclei and insular cortex (Pare 2003). It is unsurprising, therefore, that singleunit and field potential electrophysiology studies of BLA in awake rats demonstrate responses to both gustatory (Yasoshima et al. 1995;Nishijo et al. 1998) and olfactory stimuli (Rosenkranz and Grace 2002;Sevelinges et al. 2004). These findings make the amygdala a probable neural substrate for sensory processes involving gustation and/or olfaction.Permanent lesion studies support this prediction, providing evidence that the BLA plays an important role in taste-and olfaction-related classical learning behaviors. Excitotoxic BLA lesions significantly alter taste palatability Jeganathan 1999, 2000;Touzani et al. 1997) and attenuate taste preference learning (Gilbert et al. 2003). BLA ablation also impairs learning of conditioned taste aversions (CTA) (Rollins et al. 2001;Mickley et al. 2004;Reilly 2005) and taste-potentiated odor aversions (Hatfield et al. 1992;Ferry et al. 1999;Ferry and Di Scala 2000;Sakai and Yamamoto 2001).Despite these findings, however, the involvement of BLA in basic chemosensory aversion and preference learning remains a topic of some controversy (Yamamoto et al. 1994;Reilly 2005). This is partially because the BLA dependence of CTA may vary as a function of exact experimental protocol; there is some evidence that the amygdala may be vital for the formation of aversions to tastes delivered to a passive rat (i.e., via intra-oral cannulae, or IOC), but not f...

Structural and functional neural adaptations in obstructive sleep apnea: An activation likelihood estimation meta-analysis

“…In animals, amygdala has been shown as vital for learning procedures and stress-induced conditioning that involves pairings of potent and arbitrary chemosensory stimuli (Wang et al, 2006). For example, an animal study demonstrated that corticotropin-releasing factor receptors within the basolateral amygdala are involved in regulating fear-conditioned alterations in sleep (Wellman et al, 2013).…”

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

“…This difference is an important one, because approach behaviors activate a broad set of neural systems in anticipation of taste delivery (Yamamoto et al, 1988;Gutierrez et al, 2006). Anticipation changes basic aspects of taste activity (Nitschke et al, 2006), greatly decreasing the latency of taste responses in GC (Stapleton et al, 2006) and changing the circuits involved in CTA Wang et al, 2006). In an operant conditioning paradigm, we would expect palatability processing and learning-related response plasticity to both have shorter poststimulus latencies.…”

“…Conditioned taste aversion (CTA), a simple learning paradigm whereby a formerly preferred taste becomes unpalatable after being paired with gastric distress (Nachman and Ashe, 1973;Bermudez-Rattoni et al, 1986;Gallo et al, 1992;Rollins et al, 2001), offers a unique window into systems-level properties of learning, because it vitally involves both basolateral amygdala (BLA) (Nachman and Ashe, 1974;Rollins et al, 2001;Reilly and Bornovalova, 2005;Wang et al, 2006) and gustatory cortex (GC) (Gallo et al, 1992;Berman and Dudai, 2001;Stone et al, 2005), and because the speed with which taste aversions are learned makes it feasible to maintain isolations of single neurons from before until after learning using chronic microwire techniques (Katz et al, 2001b).…”

Differential Effects of Estrogen Receptor Alpha and Beta Specific Agonists on Social Learning of Food Preferences in Female Mice

“…DA has been shown to be involved in social learning, as studies in mice have found that dopamine acting on the D1 but not the D2 dopamine receptor mediates the STFP (Choleris et al, in preparation). Mesocorticolimbic DA projections innervate many of the areas known to be involved in the STFP, such as the hippocampal region, the orbitofrontal cortex, and the amygdala (eg Bunsey and Eichenbaum, 1995;Alvarez et al, 2001;Sánchez-Andrade et al, 2005;Ross et al, 2005;Wang et al, 2007). The dopaminergic system is modulated by estrogens, both through increasing the release of DA (McDermott et al, 1994;Liu and Xie, 2004) and through decreasing the expression and activity of the DA transporter, which eliminates DA from the extracellular space (Karakaya et al, 2007).…”