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The Journal of Neuroscience, March 12, 2008, 28(11):2864-2873; doi:10.1523/JNEUROSCI.4063-07.2008

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Behavioral/Systems/Cognitive
Learning-Related Plasticity of Temporal Coding in Simultaneously Recorded Amygdala–Cortical Ensembles

Stephen E. Grossman,^1,3 Alfredo Fontanini,^1,2,3 Jeffrey S. Wieskopf,³ and Donald B. Katz^1,2,3

¹Volen National Center for Complex Systems, ²Department of Psychology, and ³Program in Neuroscience, Brandeis University, Waltham, Massachusetts 02454

Correspondence should be addressed to Donald B. Katz, Volen National Center for Complex Systems, MS 013, Brandeis University, 415 South Street, Waltham, MA 02454. Email: dbkatz{at}brandeis.edu

Emotional learning requires the coordinated action of neural populations in limbic and cortical networks. Here, we performed simultaneous extracellular recordings from gustatory cortical (GC) and basolateral amygdalar (BLA) neural ensembles as awake, behaving rats learned to dislike the taste of saccharin [via conditioned taste aversion (CTA)]. Learning-related changes in single-neuron sensory responses were observed in both regions, but the nature of the changes was region specific. In GC, most changes were restricted to relatively late aspects of the response (starting 1.0 s after stimulus administration), supporting our hypothesis that in this paradigm palatability-related information resides exclusively in later cortical responses. In contrast, and consistent with data suggesting the amygdala's primary role in judging stimulus palatability, CTA altered all components of BLA taste responses, including the earliest. Finally, learning caused dramatic increases in the functional connectivity (measured in terms of cross-correlation peak heights) between pairs of simultaneously recorded BLA and GC neurons, increases that were evident only during taste processing. Our simultaneous assays of the activity of single neurons in multiple relevant brain regions across learning suggest that the transmission of taste information through amygdala–cortical circuits plays a vital role in CTA memory formation.

Key words: taste; gustatory cortex; basolateral amygdala; conditioned taste aversion; single-unit; electrophysiology

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Received Sept. 5, 2007; revised Feb. 4, 2008; accepted Feb. 5, 2008.

Correspondence should be addressed to Donald B. Katz, Volen National Center for Complex Systems, MS 013, Brandeis University, 415 South Street, Waltham, MA 02454. Email: dbkatz{at}brandeis.edu

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