Format

Send to

Choose Destination
J Neurosci. 2019 Feb 13;39(7):1195-1205. doi: 10.1523/JNEUROSCI.2492-18.2018. Epub 2018 Dec 26.

Selective Strengthening of Intracortical Excitatory Input Leads to Receptive Field Refinement during Auditory Cortical Development.

Sun YJ1,2, Liu BH1,2, Tao HW3,4, Zhang LI3,4.

Author information

1
Zilkha Neurogenetic Institute.
2
Graduate Program in Physiology and Biophysics, Keck School of Medicine, University of Southern California, Los Angeles, California 90089.
3
Zilkha Neurogenetic Institute, liizhang@usc.edu htao@usc.edu.
4
Department of Physiology and Neuroscience, and.

Abstract

In the primary auditory cortex (A1) of rats, refinement of excitatory input to layer (L)4 neurons contributes to the sharpening of their frequency selectivity during postnatal development. L4 neurons receive both feedforward thalamocortical and recurrent intracortical inputs, but how potential developmental changes of each component can account for the sharpening of excitatory input tuning remains unclear. By combining in vivo whole-cell recording and pharmacological silencing of cortical spiking in young rats of both sexes, we examined developmental changes at three hierarchical stages: output of auditory thalamic neurons, thalamocortical input and recurrent excitatory input to an A1 L4 neuron. In the thalamus, the tonotopic map matured with an expanded range of frequency representations, while the frequency tuning of output responses was unchanged. On the other hand, the tuning shape of both thalamocortical and intracortical excitatory inputs to a L4 neuron became sharpened. In particular, the intracortical input became better tuned than thalamocortical excitation. Moreover, the weight of intracortical excitation around the optimal frequency was selectively strengthened, resulting in a dominant role of intracortical excitation in defining the total excitatory input tuning. Our modeling work further demonstrates that the frequency-selective strengthening of local recurrent excitatory connections plays a major role in the refinement of excitatory input tuning of L4 neurons.SIGNIFICANCE STATEMENT During postnatal development, sensory cortex undergoes functional refinement, through which the size of sensory receptive field is reduced. In the rat primary auditory cortex, such refinement in layer (L)4 is mainly attributed to improved selectivity of excitatory input a L4 neuron receives. In this study, we further examined three stages along the hierarchical neural pathway where excitatory input refinement might occur. We found that developmental refinement takes place at both thalamocortical and intracortical circuit levels, but not at the thalamic output level. Together with modeling results, we revealed that the optimal-frequency-selective strengthening of intracortical excitation plays a dominant role in the refinement of excitatory input tuning.

KEYWORDS:

auditory cortex; developmental refinement; synaptic circuit mechanism; thalamocortical projection; tonal receptive field; whole-cell recording

Supplemental Content

Full text links

Icon for HighWire Icon for PubMed Central
Loading ...
Support Center