Distinct Subtypes of Basolateral Amygdala Taste Neurons Reflect Palatability and Reward

Abstract

The amygdala processes multiple, dissociable properties of sensory stimuli. Given its central location within a dense network of reciprocally connected regions, it is reasonable to expect that basolateral amygdala (BLA) neurons should produce a rich repertoire of dynamical responses to taste stimuli. Here, we examined single BLA neuron taste responses in awake rats and report the existence of two distinct subgroups of BLA taste neurons operating simultaneously during perceptual processing. One neuron type produced long, protracted responses with dynamics that were strikingly similar to those previously observed in gustatory cortex. These responses reflect cooperation between amygdala and cortex for the purposes of processing palatability. A second type of BLA taste neuron may be part of the system often described as being responsible for reward learning: these neurons produced very brief, short-latency responses to rewarding stimuli; when the rat participated in procuring the taste by pressing a lever in response to a tone, however, those phasic taste responses vanished, phasic responses to the tone appearing instead. Our data provide strong evidence that the neural handling of taste is actually a distributed set of processes and that BLA is a nexus of these multiple processes. These results offer new insights into how amygdala imbues naturalistic sensory stimuli with value.

State Dependency of Chemosensory Coding in the Gustatory Thalamus (VPMpc) of Alert Rats

“…The following tastants were used: 100 mM NaCl (N), 100 mM sucrose (S), 200 or 100 mM citric acid (C), and 1 mM quinine HCl (Q). Water was not delivered as a stimulus for technical reasons (because of diameter limitation, we could use only 4 polyimide tubing for the manifold) and for consistency with previous work from our and other laboratories in alert rats (Katz et al, 2001;Fontanini and Katz, 2006;Piette et al, 2012;Sadacca et al, 2012;Samuelsen et al, 2012;Gardner and Fontanini, 2014). Tastants were delivered in pseudorandom order following each cued, head entry.…”

“…All implants were cemented to the skull with dental acrylic. Intraoral cannulae (IOC) (Phillips and Norgren, 1970) were implanted bilaterally and cemented onto the head cap with dental acrylic (Katz et al, 2001;Fontanini and Katz, 2005). Rats received antibiotic treatment (topical: Neosporin ointment, Pfizer; systemic: penicillin benzathine) and analgesics (procaine and ketorolac) immediately after the surgery and for up to 4 d following the surgery.…”

“…After recovery from surgery, rats were water restricted (45 min of water/d) for ϳ5 d and habituated to the behavioral/recording chamber (MED Associates) as well as to receiving fluids through IOC (Phillips and Norgren, 1970;Katz et al, 2001;Fontanini and Katz, 2005) for 2-3 d. Once habituated, rats were trained to self-administer and passively receive tastants. In our experiments, training lasted ϳ2 weeks (i.e., until rats showed stable behavior and self-delivered Ͼ6 trials for each taste).…”

“…As measure of palatability-related information, we used a PI, as shown in previous work Fontanini et al, 2009;Jezzini et al, 2013). This method considers the difference in evoked activity between taste stimuli with similar and opposite palatability.…”

“…Neurons in GC (Yamamoto et al, 1985;Accolla and Carleton, 2008;Grossman et al, 2008;Sadacca et al, 2012), mPFC (Jezzini et al, 2013), BLA (Fontanini et al, 2009), and other taste-related regions (Li et al, 2013;Weiss et al, 2014) have been shown to encode information about taste palatability. Recordings from anesthetized rats suggested the presence of a possible "hedonic tone" in VPMpc as well (Verhagen et al, 2003).…”