Hearing loss differentially affects thalamic drive to two cortical interneuron subtypes

Abstract

Sensory deprivation, such as developmental hearing loss, leads to an adjustment of synaptic and membrane properties throughout the central nervous system. These changes are thought to compensate for diminished sound-evoked activity. This model predicts that compensatory changes should be synergistic with one another along each functional pathway. To test this idea, we examined the excitatory thalamic drive to two types of cortical inhibitory interneurons that display differential effects in response to developmental hearing loss. The inhibitory synapses made by fast-spiking (FS) cells are weakened by hearing loss, whereas those made by low threshold-spiking (LTS) cells remain strong but display greater short-term depression (Takesian et al. 2010). Whole-cell recordings were made from FS or LTS interneurons in a thalamocortical brain slice, and medial geniculate (MG)-evoked postsynaptic potentials were analyzed. Following hearing loss, MG-evoked net excitatory potentials were smaller than normal at FS cells but larger than normal at LTS cells. Furthermore, MG-evoked excitatory potentials displayed less short-term depression at FS cells and greater short-term depression at LTS cells. Thus deprivation-induced adjustments of excitatory synapses onto inhibitory interneurons are cell-type specific and parallel the changes made by the inhibitory afferents.

Cortical Interneurons Differentially Regulate the Effects of Acoustic Context

“…Another potential mechanism, modeled here, is that Sst+ and Pvalb+ interneurons are recruited by feedforward inputs with different dynamics. In both somatosensory and auditory cortical slices, inputs onto Sst+ interneurons facilitate and inputs onto Pvalb+ cells depress when stimulated at rates similar to the onset asynchrony of the tones presented in the current study (10–60 Hz; Beierlein et al, 2003; Takesian et al, 2013; Tan et al, 2008). Thus, Sst+ cells may be robustly and persistently activated during repeated sensory stimulation, allowing them to directly suppress their targets across multiple stimulations.…”

“…In vitro, Sst+ cells receive mostly facilitating inputs, whereas Pvalb+ cells receive mostly depressing inputs (Beierlein et al, 2003; Takesian et al, 2013; Tan et al, 2008)—a potential mechanism for their distinct effects on forward suppression. Thus, we modeled the influences of interneuron populations with either depressing or facilitating inputs on responses in a two-tone paradigm.…”

Experience-Dependent Bimodal Plasticity of Inhibitory Neurons in Early Development

“…In mouse visual cortex, connections from layer 4 fast spiking neurons and regular spiking non-pyramidal neurons to pyramidal neurons undergo different visual deprivation induced homeostatic modifications (Maffei et al, 2004). Similarly, developmental auditory deprivation results in cell type- and pathway-specific homeostatic plasticity of inhibitory circuits (Takesian et al, 2010; Takesian et al, 2013). In agreement with these reports, we find two functionally distinct inhibitory neuron populations in the developing optic tectum, distinguished by their structural and functional plasticity responses to experience.…”

Neurophysiology and Regulation of the Balance Between Excitation and Inhibition in Neocortical Circuits

“…Plasticity can also be induced at afferent inputs (39), altering how local excitatory and inhibitory circuits become engaged by an incoming stimulus (40). Feedforward projections such as thalamocortical afferents synapse on both excitatory and inhibitory neurons (41).…”