Elsevier

Neuroscience

Volume 145, Issue 3, 30 March 2007, Pages 832-840
Neuroscience

Behavioural neuroscience
Environmental enrichment selectively increases glutamatergic responses in layer II/III of the auditory cortex of the rat

https://doi.org/10.1016/j.neuroscience.2006.12.061Get rights and content

Abstract

Prolonged exposure to environmental enrichment (EE) induces behavioral adaptation accompanied by detectable morphological and physiological changes. Auditory EE is associated with an increased auditory evoked potential (AEP) and increased auditory gating in the primary auditory cortex. We sought physiological correlates to such changes by comparing synaptic currents in control vs. EE-raised rats, in a primary auditory cortex (AI) slice preparation. Pharmacologically isolated glutamatergic or GABAA-receptor-mediated currents were measured using perforated patch whole-cell recordings. Glutamatergic AMPA receptor (AMPAR)-mediated excitatory postsynaptic currents (EPSCs) displayed a large amplitude increase (64±11% in EE vs. control) accompanied by a rise-time decrease (−29±6% in EE vs. control) and decrease in pair pulse ratio in layer II/III but not in layer V. Changes in glutamatergic signaling were not associated with changes in the ratio between N-methyl-d aspartate-receptor (NMDAR)-mediated vs. AMPAR-mediated components, in amplitude or pair pulse ratio of GABAergic transmission, or in passive neuronal properties.

A realistic computational model was used for integrating in vivo and in vitro results, and for determining how EE synapses correct for phase error of the inputs. We found that EE not only increases the mean firing frequency of the responses, but also improves the robustness of auditory processing by decreasing the dependence of the output firing on the phase difference of the input signals.

We conclude that behavioral and electrophysiological differences detected in vivo in rats exposed to an auditory EE are accompanied and possibly caused by selective changes in cortical excitatory transmission. Our data suggest that auditory EE selectively enhances excitatory glutamatergic synaptic transmission in layer II/III without greatly altering inhibitory GABAergic transmission.

Section snippets

Environmental conditions

Twenty-three control and 27 EE-raised Sprague–Dawley rats were used in this study. All rats were housed with their mothers and littermates until they reached an age of 21 days. They were then randomly separated and placed into either enriched or standard housing conditions. Rats were given a code of colored tail stripes in order to preserve their housing condition’s confidentiality from experimenters and avoid any unintentional bias. All rats were provided with food and water ad libitum. A

AMPAR-mediated currents in layer II/III

Since EE increases 3H AMPA binding in the hippocampus (Foster et al., 1996) and has been suggested to enhance glutamatergic activity (Foster and Dumas, 2001), we first measured the amplitude of electrically evoked EPSCs in visually identified neurons from layer II/III of the auditory cortex. A paired pulse protocol was applied with an interpulse delay varying between 20 and 1000 ms, for evaluating possible presynaptic differences between EE and the control group. In order to avoid a possible

Discussion

The influence of the environment on animal behavior has long been documented. Several anatomical and physiological studies have clearly demonstrated an involvement of the hippocampus and related structures (Green and Greenough 1986, Foster et al 2000, Sharp et al 1985, Faherty et al 2003, Foster and Dumas 2001). Recently more attention has been focused on how EE affects other brain areas, including the neocortex (Nithianantharajah et al., 2004). In particular, large anatomical rearrangements of

Acknowledgments

J.A.N. performed most of the patch-clamp experiments, analyzed and elaborated data and figures, and contributed to writing the final version of the manuscript, V.P.J. raised the EE animals and contributed to the discussion, H.S. recorded part of the mEPSC and of the APV experiments, L.D. wrote and ran the MatLab program using literature and original data, M.P.K. contributed to the original idea, to the design of the experiments and to the final version of the manuscript, M.A. contributed to the

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