Correspondence should be addressed to Emma C. 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.
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Correspondence should be addressed to Emma C. 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. 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. Keywords: associative learning, auditory cortex, inhibition, synaptic plasticity Introduction The representation of sound in auditory cortex can be modified by both chronic environmental conditions and learning for review, see Keuroghlian and Knudsen, ; Sanes and Bao, ; de Villers-Sidani and Merzenich, ; Schreiner and Polley, For example, learning to detect a spectral cue or discriminate a spectral cue from among other cue causes 1 cortical single-neuron receptive fields to shift rapidly and persistently toward the conditioned frequency, and 2 representation of relevant frequencies to expand Edeline et al.
In fact, the magnitude of reorganization is correlated with both magnitude of learning, as well as resistance to extinction Rutkowski and Weinberger, ; Bieszczad and Weinberger, Modification of functional properties is not restricted to sound frequency. Learning can also lead to altered temporal response properties or sound-level tuning to favor the features of salient sounds Bao et al.
However, learning-induced alterations of the cortical sensory representation can dissipate as animals continue to practice a task Molina-Luna et al. Thus, auditory learning is accompanied by modifications to the representation of acoustic cues in primary auditory cortex, which may facilitate behavioral sensitivity to the conditioned stimulus. Disinhibition or the reduction of inhibitory synaptic gain and the associated increase in excitability is one cellular mechanism that may facilitate long-term modification to sensory cortex processing.
In the auditory system, the experience-dependent plasticity that occurs during classical conditioning is associated with an enhancement of excitation within the auditory cortex Blake et al.
Consistent with this finding, disinhibition in the auditory cortex is necessary for a simple form of associative learning Letzkus et al. We predicted that, if inhibitory plasticity is associated with task learning, then the expression of inhibitory plasticity would emerge and persist until task proficiency was achieved, regardless of the training procedure. To examine whether adjustments to cortical GABAergic transmission accompany associative learning, we measured spontaneous GABAA receptor-mediated synaptic currents in auditory cortex brain slices obtained from gerbils undergoing daily auditory training.
Animals were trained to detect an amplitude-modulated noise, using either an aversive or an appetitive procedure. Auditory cortex brain slices were obtained on sequential days, immediately following each training session. Both presynaptic and postsynaptic measures of inhibitory function were recorded to determine whether synaptic adjustments were associated with learning, and whether they were specific to a particular training procedure.
The results showed a decrease in IPSC amplitude that coincided with the onset of associative learning in animals with auditory training, but not in control animals. In contrast, the paired-pulse ratio PPR decreased both in animals with auditory training and in controls. These results suggest that a transient decrease in inhibitory gain permit the modification of stimulus representation that accompanies learning. Materials and Methods Gerbil Meriones unguiculatus pups were weaned from commercial breeding pairs Charles River.
Animals were trained on one of two auditory tasks: either a conditioned-avoidance task or appetitive task both described in detail below. Behavior: aversive conditioning Animals were trained on a Go-Nogo conditioned-avoidance procedure to detect amplitude modulation Heffner and Heffner, ; Heffner et al. Since we were interested in the physiological changes that may occur in the same animals over the course of associative learning, we recorded cells from animals that had an increasingly greater number of training days.
Gerbils were placed in a small plastic cage in a sound-isolation booth Gretch-Ken Industries and observed from a separate room via a closed-circuit monitor.
When the animal contacted both the plate and spout, a circuit was completed that initiated water delivery via a syringe pump New Era Pump Systems. The metal lick spout was similar in appearance to that within the home cage Fig.
Cortical Synaptic Inhibition Declines during Auditory Learning
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