Developmental sensory experience balances cortical excitation and inhibition

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Abstract
In order to build a proper and stable representation of the auditory world, neonatal rodents exhibit a significant degree of circuit plasticity, allowing for sensitivity to the pattern of sensory inputs. During this time, neurons construct a receptive field, one that relies upon a particular balance of excitatory and inhibitory inputs, yet it is unknown as to how this balance is formed. Two studies published in this issue of Nature reveal contrasting views as to how the mature system develops. Excitation and inhibition were found to be equally strong upon hearing onset in each study. But whereas Dorrn et al. find evidence for an experience-dependent refinement of inhibition as the receptive fields develop, Sun et al. observed a fine adjustment in the excitatory input strength to produce a shifted balance. Nevertheless, taken together, both studies point towards a fine adjustment of synaptic inputs as the force behind the production of mature receptive fields, as opposed to more radical changes such as input pruning. To build a representation of the auditory world, neuronal circuits in neonatal rodents exhibit plasticity, allowing sensitivity to the pattern of sensory inputs. At this time, neurons construct a receptive field, which relies on a balance of excitatory and inhibitory inputs. Here, excitation and inhibition were found to be co-tuned upon hearing onset, but an experience-dependent refinement of inhibition later occurred. Thus a fine adjustment in synaptic inputs, rather than more radical changes such as input pruning, may refine mature receptive fields. Early in life, neural circuits are highly susceptible to outside influences. The organization of the primary auditory cortex (A1) in particular is governed by acoustic experience during the critical period, an epoch near the beginning of postnatal development throughout which cortical synapses and networks are especially plastic1,2,3,4,5,6,7,8. This neonatal sensitivity to the pattern of sensory inputs is believed to be essential for constructing stable and adequately adapted representations of the auditory world and for the acquisition of language skills by children5,9,10. One important principle of synaptic organization in mature brains is the balance between excitation and inhibition, which controls receptive field structure and spatiotemporal flow of neural activity11,12,13,14,15, but it is unknown how and when this excitatory–inhibitory balance is initially established and calibrated. Here we use whole-cell recording to determine the processes underlying the development of synaptic receptive fields in rat A1. We find that, immediately after the onset of hearing, sensory-evoked excitatory and inhibitory responses are equally strong, although inhibition is less stimulus-selective and mismatched with excitation. However, during the third week of postnatal development, excitation and inhibition become highly correlated. Patterned sensory stimulation drives coordinated synaptic changes across receptive fields, rapidly improves excitatory–inhibitory coupling and prevents further exposure-induced modifications. Thus, the pace of cortical synaptic receptive field development is set by progressive, experience-dependent refinement of intracortical inhibition.