Cortical Synaptic Inhibition Declines during Auditory Learning

Abstract

Auditory learning is associated with an enhanced representation of acoustic cues in primary auditory cortex, and modulation of inhibitory strength is causally involved in learning. If this inhibitory plasticity is associated with task learning and improvement, its expression should emerge and persist until task proficiency is achieved. We tested this idea by measuring changes to cortical inhibitory synaptic transmission as adult gerbils progressed through the process of associative learning and perceptual improvement. Using either of two procedures, aversive or appetitive conditioning, animals were trained to detect amplitude-modulated noise and then tested daily. Following each training session, a thalamocortical brain slice was generated, and inhibitory synaptic properties were recorded from layer 2/3 pyramidal neurons. Initial associative learning was accompanied by a profound reduction in the amplitude of spontaneous IPSCs (sIPSCs). However, sIPSC amplitude returned to control levels when animals reached asymptotic behavioral performance. In contrast, paired-pulse ratios decreased in trained animals as well as in control animals that experienced unpaired conditioned and unconditioned stimuli. This latter observation suggests that inhibitory release properties are modified during behavioral conditioning, even when an association between the sound and reinforcement cannot occur. These results suggest that associative learning is accompanied by a reduction of postsynaptic inhibitory strength that persists for several days during learning and perceptual improvement.

Region- and Layer-Specific Activation of the Higher Order Auditory Cortex Te2 after Remote Retrieval of Fear or Appetitive Memories

“…Further studies confirmed the recruitment of layer II/III interneurons in auditory fear memory in mice (Pi et al 2013;Sarro et al 2015) Changes in neuronal activity have also been detected in superficial layers during spatial (Maviel et al 2004) and other hippocampal-dependent (Frankland et al 2004;Lesburguères et al 2011) tasks in both rats and mice brain cortices, including the prefrontal, anterior cingulate, parietal and temporal cortices (Frankland and Bontempi 2005). Spine remodeling and growth has been shown to occur in superficial layers during remote memory formation in mice (Lesburguères et al 2011;Vetere et al 2011;Xie et al 2014), and contextual fear conditioning has been shown to determine a memory-related activation of sparse neurons in layer II of several cortices in mice, which lasts for 2 months (Xie et al 2014).…”

Top-down modulation of sensory cortex gates perceptual learning

“…AM detection was assessed with an aversive conditioning paradigm as described previously (29,87,88). Psychometric functions were fit with cumulative Gaussians and transformed to the signal detection metric, d′ (89).…”

“…The neural basis of PL has commonly been evaluated by focusing on two time points (pre-vs. posttraining) or groups (trained vs. untrained) (6-12, 14-16, 30). However, training-based perceptual improvement can be associated with transient phases of functional plasticity, even within a single network (26)(27)(28)(29). Thus, studies that are restricted to one or two time points could fail to identify a temporary contribution of a particular brain region to PL.…”

“…For example, some neural changes associated with PL are transient (26)(27)(28)(29), making it necessary to monitor neural activity throughout the duration of perceptual training, rather than making comparisons only after PL is complete (6-12, 14-16, 30). For similar reasons, it is critical to block the function of a specific candidate brain region during training to determine whether it plays a causal role in PL.…”

Developmental hearing loss impedes auditory task learning and performance in gerbils

“…For CHL animals, identical stimuli were used however they were presented at 95 dB SPL (i.e., 45 dB louder than that used for NH animals), to compensate for the induced loss. Except for the sound level used for CHL animals, all general training and testing procedures were similar to those described previously for NH animals (Buran et al, 2014b; Sarro et al, 2015). …”