Experience-dependent plasticity in the brain requires balanced excitation-inhibition. How individual circuit elements contribute to plasticity outcome in complex neocortical networks remains unknown. Here we report an intracellular analysis of ocular dominance plasticity-the loss of acuity and cortical responsiveness for an eye deprived of vision in early life. Unlike the typical progressive loss of pyramidal-cell bias, direct recording from fast-spiking cells in vivo reveals a counterintuitive initial shift towards the occluded eye followed by a late preference for the open eye, consistent with a spike-timing-dependent plasticity rule for these inhibitory neurons. Intracellular pharmacology confirms a dynamic switch of GABA (gamma-aminobutyric acid) impact to pyramidal cells following deprivation in juvenile mice only. Together these results suggest that the bidirectional recruitment of an initially binocular GABA circuit may contribute to experience-dependent plasticity in the developing visual cortex.

Summary What causes critical periods (CPs) to open? For the best-studied case, ocular dominance plasticity in primary visual cortex in response to monocular deprivation (MD), the maturation of inhibition is necessary and sufficient. How does inhibition open the CP? We present a novel theory: the transition from pre-CP to CP plasticity arises because inhibition preferentially suppresses responses to spontaneous relative to visually-driven input activity, switching learning cues from internal to external sources. This differs from previous proposals in (1) arguing that the CP can open without changes in plasticity mechanisms when, through circuit development, activity patterns become more sensitive to sensory experience; (2) explaining not simply a transition from no plasticity to plasticity, but rather the change in outcome of MD-induced plasticity,from pre-CP to CP,. More broadly, hierarchical organization of sensory-motor pathways may develop through a cascade of CPs induced as circuit maturation progresses from “lower” to “higher” cortical areas.

As in human speech acquisition, songbird vocal learning depends on early auditory experience. During development, juvenile songbirds listen to and form auditory memories of adult tutor songs, which they use to shape their own vocalizations in later sensorimotor learning. The higher-level auditory cortex, called the caudomedial nidopallium (NCM), is a potential storage site for tutor song memory, but no direct electrophysiological evidence of tutor song memory has been found. Here, we identify the neuronal substrate for tutor song memory by recording single-neuron activity in the NCM of behaving juvenile zebra finches. After tutor song experience, a small subset of NCM neurons exhibit highly selective auditory responses to the tutor song. Moreover, blockade of GABAergic inhibition, and sleep decrease their selectivity. Taken together, these results suggest that experience-dependent recruitment of GABA-mediated inhibition shapes auditory cortical circuits, leading to sparse representation of tutor song memory in auditory cortical neurons.

Juvenile songbirds learn vocal communication from adult tutors of the same species but not from adults of other species. How species-specific learning emerges from the basic features of song prosody remains unknown. In the zebra finch auditory cortex, we discovered a class of neurons that register the silent temporal gaps between song syllables and are distinct from neurons encoding syllable morphology. Behavioral learning and neuronal coding of temporal gap structure resisted song tutoring from other species: Zebra finches fostered by Bengalese finch parents learned Bengalese finch song morphology transposed onto zebra finch temporal gaps. During the vocal learning period, temporal gap neurons fired selectively to zebra finch song. The innate temporal coding of intersyllable silent gaps suggests a neuronal barcode for conspecific vocal learning and social communication in acoustically diverse environments.

Yazaki-Sugiyama, Yoko and Richard Mooney. Sequential learning from multiple tutors and serial retuning of auditory neurons in a brain area important to birdsong learning. J Neurophysiol 92: 2771-2788, 2004. First published June 30, 2004 10.1152/jn.00467.2004. Songbirds hear many vocal models during a juvenile sensitive period, transiently imitating some while retaining imitations of others in their repertoires. Despite subsequent conflicting experiences, early experience can exert lasting effects on neural structure and function, raising the possibility that transiently expressed vocalizations or their relevant models are stored in the adult songbird's brain. One site where learned song representations could be stored is the lateral magnocellular nucleus of the anterior nidopallium (LMAN), which in the adult songbird contains neurons responsive to playback of the bird's own song (BOS) and the tutor song (TS). To test whether LMAN neurons develop and retain responses to transiently learned songs, we exposed zebra finch hatchlings [posthatch day 0 (PHD0)] to a first TS (TS1) for about 30 days, isolated them for about 30 days, then exposed them to a second TS (TS2) for 30 days starting at PHD 60. Behavioral analysis showed that PHD 60 juveniles had started to copy TS1, although this copying was transient, because the adult BOS resembled TS2 and not TS1. We found that LMAN auditory responses paralleled these behavioral changes: LMAN neurons at PHD 60 responded strongly and selectively to both the juvenile BOS and TS1, whereas LMAN neurons in adults responded to the adult BOS and TS2, but not to the transiently learned song or its model. Therefore LMAN auditory responses can be lost or overwritten as the juvenile copies a new song, suggesting that the adult LMAN does not store information about transiently learned songs or their models.