Environmental enrichment produces a behavioral phenotype mediated by low cyclic adenosine monophosphate response element binding (CREB) activity in the nucleus accumbens

Biol Psychiatry. 2010 Jan 1;67(1):28-35. doi: 10.1016/j.biopsych.2009.06.022.

Abstract

Background: Previous research has shown that rats reared in an enriched condition (EC) are more sensitive to the acute effects of amphetamine than rats reared in an isolated condition (IC); yet, EC rats self-administer less amphetamine than IC rats. The present study used cocaine to further explore this environmental enrichment behavioral phenotype, as well as the underlying molecular mechanisms involved.

Methods: Enriched condition and IC rats were studied in a broad battery of behavioral tests, including cocaine conditioned place preference (CPP) and self-administration and several measures of anxiety- and depression-related behavior. The involvement of the transcription factor, cyclic adenosine monophosphate (cAMP) response element binding protein (CREB), in mediating EC versus IC differences was investigated.

Results: Enriched condition rats exhibited less cocaine self-administration, despite showing enhanced cocaine CPP. Enriched condition rats also displayed less depression-like behavior but higher levels of anxiety-like behavior. This behavioral phenotype is consistent with low CREB activity in the nucleus accumbens, a key brain reward region. Indeed, EC rats have less phospho-CREB (the transcriptionally active form of the protein) in the nucleus accumbens than IC rats, and a selective knockdown of CREB in this brain region of normally reared rats, by use of a novel viral vector expressing a short hairpin RNA (shRNA) directed against CREB, reproduced the EC behavioral phenotype.

Conclusions: These studies identify a potential molecular mechanism for how rearing environment-a nonpharmacological, nonsurgical manipulation-can modify a wide range of complex emotional behaviors.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Analysis of Variance
  • Animals
  • Animals, Newborn
  • Anxiety / metabolism
  • Anxiety / pathology
  • Behavior, Animal / physiology
  • Behavioral Symptoms* / metabolism
  • Behavioral Symptoms* / pathology
  • Behavioral Symptoms* / physiopathology
  • Brain-Derived Neurotrophic Factor / genetics
  • Brain-Derived Neurotrophic Factor / metabolism
  • CREB-Binding Protein / genetics
  • CREB-Binding Protein / metabolism*
  • Cocaine / administration & dosage
  • Conditioning, Operant / drug effects
  • Depression / metabolism
  • Depression / pathology
  • Disease Models, Animal
  • Dopamine Uptake Inhibitors / administration & dosage
  • Dose-Response Relationship, Drug
  • Environment*
  • Food Preferences / physiology
  • Male
  • Nucleus Accumbens / drug effects
  • Nucleus Accumbens / metabolism*
  • Phenotype*
  • RNA, Messenger / metabolism
  • RNA, Small Interfering / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Reinforcement Schedule
  • Self Administration

Substances

  • Brain-Derived Neurotrophic Factor
  • Dopamine Uptake Inhibitors
  • RNA, Messenger
  • RNA, Small Interfering
  • CREB-Binding Protein
  • Cocaine