β-adrenergic modulation of discrimination learning and memory in the auditory cortex

Eur J Neurosci. 2019 Oct;50(7):3141-3163. doi: 10.1111/ejn.14480. Epub 2019 Jul 1.

Abstract

Despite vast literature on catecholaminergic neuromodulation of auditory cortex functioning in general, knowledge about its role for long-term memory formation is scarce. Our previous pharmacological studies on cortex-dependent frequency-modulated tone-sweep discrimination learning of Mongolian gerbils showed that auditory-cortical D1/5 -dopamine receptor activity facilitates memory consolidation and anterograde memory formation. Considering overlapping functions of D1/5 -dopamine receptors and β-adrenoceptors, we hypothesised a role of β-adrenergic signalling in the auditory cortex for sweep discrimination learning and memory. Supporting this hypothesis, the β1/2 -adrenoceptor antagonist propranolol bilaterally applied to the gerbil auditory cortex after task acquisition prevented the discrimination increment that was normally monitored 1 day later. The increment in the total number of hurdle crossings performed in response to the sweeps per se was normal. Propranolol infusion after the seventh training session suppressed the previously established sweep discrimination. The suppressive effect required antagonist injection in a narrow post-session time window. When applied to the auditory cortex 1 day before initial conditioning, β1 -adrenoceptor-antagonising and β1 -adrenoceptor-stimulating agents retarded and facilitated, respectively, sweep discrimination learning, whereas β2 -selective drugs were ineffective. In contrast, single-sweep detection learning was normal after propranolol infusion. By immunohistochemistry, β1 - and β2 -adrenoceptors were identified on the neuropil and somata of pyramidal and non-pyramidal neurons of the gerbil auditory cortex. The present findings suggest that β-adrenergic signalling in the auditory cortex has task-related importance for discrimination learning of complex sounds: as previously shown for D1/5 -dopamine receptor signalling, β-adrenoceptor activity supports long-term memory consolidation and reconsolidation; additionally, tonic input through β1 -adrenoceptors may control mechanisms permissive for memory acquisition.

Keywords: ICI118,551; Mongolian gerbil; acquisition; atenolol; clenbuterol; consolidation; isoproterenol; propranolol; reconsolidation; xamoterol.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acoustic Stimulation
  • Adrenergic beta-1 Receptor Agonists / administration & dosage
  • Adrenergic beta-2 Receptor Antagonists / administration & dosage
  • Animals
  • Auditory Cortex / physiology*
  • Discrimination Learning / physiology*
  • Gerbillinae
  • Male
  • Memory / physiology*
  • Propranolol / administration & dosage
  • Receptors, Adrenergic, beta-1 / physiology*
  • Receptors, Adrenergic, beta-2 / physiology*

Substances

  • Adrenergic beta-1 Receptor Agonists
  • Adrenergic beta-2 Receptor Antagonists
  • Receptors, Adrenergic, beta-1
  • Receptors, Adrenergic, beta-2
  • Propranolol