The neural system underlying conditioned taste aversion (CTA) is, like all systems underlying perceptual learning, highly complex-learning-relevant regions, most notably including basolateral amygdala (BLA) and gustatory cortex (GC), reciprocally innervate one another and then feedback on their brainstem sources of information. While most research to date has focused on the influence of each region separately rather than on their influence on each other, my lab's work is a direct investigation of inter- neuronal and inter-regional interactions during taste learning. This work has identified learning- dependent coupling between BLA and GC taste responses, each of which shifts at ~ 0.2 sec and ~0.6- 0.8 sec, and has gone on to show that CTA causes changes in GC firing that are restricted to the period following that second shift-firing that tracks taste palatability across both learning and extinction. BLA activity has been shown to be vital for this emergence of palatability-related firing, suggesting-but not proving-that BLA-GC axons are particularly vital for learning. The experiments proposed here will greatly enrich this foundational understanding of how amygdala and cortex work together during perceptual learning. We will acutely and selectively inhibit firing in neurons that project to GC from BLA, and test whether this perturbation: 1) is sufficient to block CTA learning; and 2) affects learning- and behavior-linked aspects of GC population responses appropriately (and in lock-step with perception). We will then do the inverse experiment, testing whether the impact of BLA-GC axons on learning-related population activity is itself modulated by activity in the GC-BLA pathway. Finally, we will examine the degree to which this amygdalo-cortical cooperation, and the coherent population activity that it engenders, is a function of cholinergic input from the nucleus basalis-input that is known to be important for learning, and that has been specifically proposed to mediate coherent firing in neuronal ensembles-by selectively perturbing this modulatory input (using ChAT::cre+ rats) during CTA training (coincident with recordings). Together, these experiments will directly test an uniquely systems-level view of perceptual learning, in the process revealing the neural mechanisms of a more general experiential phenomenon that affects (sometimes adversely) all mammals including humans.

Public Health Relevance

When a taste is placed on our tongues, we must decide whether to push it to the back for swallowing or to the front for ejecting, a decision that depends on our experience with the taste. The process whereby we learn to reject a potentially harmful taste involves the amygdala and cortex, reciprocally connected forebrain structures. The novel work proposed in this grant will rigorously test whether axons connecting amygdalar neurons to cortex play a specific role in learning and the formation of learning-related cortical response plasticity, and how that role is supported. The more systemic understanding of taste learning that will emerge from this research will help us to develop tools to aid parents with a wide range of child feeding issues, and to cure vexing taste abnormalities such as develop during pregnancy.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
5R01DC006666-14
Application #
9604795
Study Section
Neurobiology of Learning and Memory Study Section (LAM)
Program Officer
Sullivan, Susan L
Project Start
2004-01-01
Project End
2020-11-30
Budget Start
2018-12-01
Budget End
2019-11-30
Support Year
14
Fiscal Year
2019
Total Cost
Indirect Cost
Name
Brandeis University
Department
Psychology
Type
Schools of Arts and Sciences
DUNS #
616845814
City
Waltham
State
MA
Country
United States
Zip Code
02453
Flores, Veronica L; Parmet, Tamar; Mukherjee, Narendra et al. (2018) The role of the gustatory cortex in incidental experience-evoked enhancement of later taste learning. Learn Mem 25:587-600
Flores, Veronica L; Moran, Anan; Bernstein, Max et al. (2016) Preexposure to salty and sour taste enhances conditioned taste aversion to novel sucrose. Learn Mem 23:221-8
Baez-Santiago, Madelyn A; Reid, Emily E; Moran, Anan et al. (2016) Dynamic taste responses of parabrachial pontine neurons in awake rats. J Neurophysiol 115:1314-23
Sadacca, Brian F; Mukherjee, Narendra; Vladusich, Tony et al. (2016) The Behavioral Relevance of Cortical Neural Ensemble Responses Emerges Suddenly. J Neurosci 36:655-69
Levitan, David; Fortis-Santiago, Yaihara; Figueroa, Joshua A et al. (2016) Memory Retrieval Has a Dynamic Influence on the Maintenance Mechanisms That Are Sensitive to ?-Inhibitory Peptide (ZIP). J Neurosci 36:10654-10662
Li, Jennifer X; Maier, Joost X; Reid, Emily E et al. (2016) Sensory Cortical Activity Is Related to the Selection of a Rhythmic Motor Action Pattern. J Neurosci 36:5596-607
Maier, Joost X; Blankenship, Meredith L; Li, Jennifer X et al. (2015) A Multisensory Network for Olfactory Processing. Curr Biol 25:2642-50
Moran, Anan; Katz, Donald B (2014) Sensory cortical population dynamics uniquely track behavior across learning and extinction. J Neurosci 34:1248-57
Pavão, Rodrigo; Piette, Caitlin E; Lopes-dos-Santos, Vítor et al. (2014) Local field potentials in the gustatory cortex carry taste information. J Neurosci 34:8778-87
Monk, Kevin J; Rubin, Benjamin D; Keene, Jennifer C et al. (2014) Licking microstructure reveals rapid attenuation of neophobia. Chem Senses 39:203-13

Showing the most recent 10 out of 29 publications