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

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 GABA(A)-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.

Environmental enrichment increases amphetamine-induced glutamate neurotransmission in the nucleus accumbens: A neurochemical study

“…However, given that the amphetamine-induced increase in glutamate was blocked completely by MK-801 in EC rats, an involvement of NMDA receptors is implicated. Consistent with this, compared to IC rats, EC rats have increased glutamate transmission in cortex and hippocampus (Nichols et al, 2007;Segovia et al, 2006) and decreased expression of NMDA receptor subunits in NAcc (Wood et al, 2005). The decrease in NMDA receptor expression in NAcc may represent a compensatory down-regulation in response to an enhanced glutamate signal.…”

Reorganization in processing of spectral and temporal input in the rat posterior auditory field induced by environmental enrichment

“…To avoid the possibility of any sex-based variability in cortical processing of sounds, we restricted our study to female rats. The enriched and standard housing conditions were identical to those in earlier reports published from our lab (Bose et al 2010;Engineer et al 2004;Kilgard et al 2007;Nichols et al 2007;Percaccio et al 2005). Rats in both environments received food and water ad libitum, were on a reverse 12:12-h light-dark cycle, and were exposed to the same constant temperature and humidity levels.…”

“…In addition, PAF bandwidths narrow to a greater extent than can be explained by direct transmission of bandwidth changes in A1, suggesting increased local stimulus-evoked surround inhibition in PAF after enrichment. The fact that basal GABA levels decrease (Sale et al 2007) but there is no decrease in evoked GABA release in primary sensory cortex (Nichols et al 2007) suggests that enrichment could affect basal and evoked GABA levels differently in the cortex. We propose that while enrichment decreases basal levels of GABA, it increases local stimulus-evoked GABAergic inhibition of pyramidal cells in PAF.…”

Environmental enrichment and the sensory brain: the role of enrichment in remediating brain injury

“…Nichols et al (2007) have shown that exposure to EE induces an AMPA-receptor mediated increase in EPSC amplitudes in supragranular layers of the auditory cortex, with no changes in GABA-ergic transmission, while the increase in PPD after EE demonstrated by Percaccio et al (2005) suggests an increase in the transmitter release probability of excitatory synapses.…”