Cell-Specific Activity-Dependent Fractionation of Layer 2/35->5B Excitatory Signaling in Mouse Auditory Cortex

Abstract

Auditory cortex (AC) layer 5B (L5B) contains both corticocollicular neurons, a type of pyramidal-tract neuron projecting to the inferior colliculus, and corticocallosal neurons, a type of intratelencephalic neuron projecting to contralateral AC. Although it is known that these neuronal types have distinct roles in auditory processing and different response properties to sound, the synaptic and intrinsic mechanisms shaping their input-output functions remain less understood. Here, we recorded in brain slices of mouse AC from retrogradely labeled corticocollicular and neighboring corticocallosal neurons in L5B. Corticocollicular neurons had, on average, lower input resistance, greater hyperpolarization-activated current (Ih), depolarized resting membrane potential, faster action potentials, initial spike doublets, and less spike-frequency adaptation. In paired recordings between single L2/3 and labeled L5B neurons, the probabilities of connection, amplitude, latency, rise time, and decay time constant of the unitary EPSC were not different for L2/3corticocollicular and L2/3corticocallosal connections. However, short trains of unitary EPSCs showed no synaptic depression in L2/3corticocollicular connections, but substantial depression in L2/3corticocallosal connections. Synaptic potentials in L2/3corticocollicular connections decayed faster and showed less temporal summation, consistent with increased Ih in corticocollicular neurons, whereas synaptic potentials in L2/3corticocallosal connections showed more temporal summation. Extracellular L2/3 stimulation at two different rates resulted in spiking in L5B neurons; for corticocallosal neurons the spike rate was frequency dependent, but for corticocollicular neurons it was not. Together, these findings identify cell-specific intrinsic and synaptic mechanisms that divide intracortical synaptic excitation from L2/3 to L5B into two functionally distinct pathways with different input-output functions.

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original_citation: Joshi A, Middleton JW, Anderson CT, Borges K, Suter BA, Shepherd GM, Tzounopoulos T. (2015) Cell-Specific Activity-Dependent Fractionation of Layer 2/35B Excitatory Signaling in Mouse Auditory Cortex. J Neurosci 35(7):3112-3123

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