The role of the gustatory cortex in incidental experience-evoked enhancement of later taste learning

Abstract

The strength of learned associations between pairs of stimuli is affected by multiple factors, the most extensively studied of which is prior experience with the stimuli themselves. In contrast, little data is available regarding how experience with "incidental" stimuli (independent of any conditioning situation) impacts later learning. This lack of research is striking given the importance of incidental experience to survival. We have recently begun to fill this void using conditioned taste aversion (CTA), wherein an animal learns to avoid a taste that has been associated with malaise. We previously demonstrated that incidental exposure to salty and sour tastes (taste preexposure-TPE) enhances aversions learned later to sucrose. Here, we investigate the neurobiology underlying this phenomenon. First, we use immediate early gene (c-Fos) expression to identify gustatory cortex (GC) as a site at which TPE specifically increases the neural activation caused by taste-malaise pairing (i.e., TPE did not change c-Fos induced by either stimulus in isolation). Next, we use site-specific infection with the optical silencer Archaerhodopsin-T to show that GC inactivation during TPE inhibits the expected enhancements of both learning and CTA-related c-Fos expression, a full day later. Thus, we conclude that GC is almost certainly a vital part of the circuit that integrates incidental experience into later associative learning.

Impact of precisely-timed inhibition of gustatory cortex on taste behavior depends on single-trial ensemble dynamics

“…Lengthy disruptions of GC activity appear to have lasting effects that can confound the interpretation of their behavioral impact - our 2.5s long optogenetic perturbations delayed the onset of gaping even in control (no-laser) trials. Such spillover effects may reflect cellular or network-level processes, but they cannot be attributed to cell death caused by the perturbation: in our case, similar optogenetic protocols have been shown to have no observable impact on cell integrity in GC, even for perturbations much longer than 2.5s (Maier et al, 2015; Flores et al, 2018); furthermore, the same rats in later sessions produced normally-timed orofacial responses on the control trials. We suggest that, to at least some degree, such effects on behavior reflect the widespread nature of taste processing, and the status of GC as one participatory node.…”

“…This output power perturbs all ArchT infected neurons in a 1mm 3 sphere below the tip of the fiber in vivo (Han et al, 2011; Yizhar et al, 2011) - a sphere that encompasses about 33% of GC in the caudal-rostral axis (Kosar et al, 1986; Maier et al, 2015; Li et al, 2016). These parameters have previously been shown to reduce the activity of ArchT+ cortical neurons with minimal latency and damage (Maier et al, 2015; Li et al, 2016; Flores et al, 2018).…”

“…The spread of AAV in GC was evaluated via the expression of GFP, as has been done previously (Maier et al, 2015; Li et al, 2016; Flores et al, 2018).…”

Perturbation of amygdala-cortical projections reduces ensemble coherence of palatability coding in gustatory cortex

“…The brains were extracted and stored in a 10% formalin/30% sucrose solution for at least 3 days, after which they were frozen and sliced on a sliding microtome (Leica SM2010R, Leica Microsystems; thickness 50 µm). Slices were stained and mounted using an established protocol ( Flores et al, 2018 ; Li et al, 2016 ), and ArchT-expression in GC and BLA was evaluated via inspection of fluorescence (eGFP) under a Keyence fluorescence microscope.…”

Perturbation of amygdala-cortical projections reduces ensemble coherence of palatability coding in gustatory cortex

“…The brains were extracted and stored in a 10% formalin / 30% sucrose solution for at least days, after which they were frozen and sliced on a sliding microtome (Leica SM2010R, Leica Microsystems; thickness 50 µm). Slices were stained and mounted using an established protocol (Flores et al 2018;Li et al 2016), and ArchT-expression in GC and BLA was evaluated via inspection of fluorescence (eGFP) under a Keyence fluorescence microscope.…”