Abstract
The mammalian sensory cortex is composed of multiple types of inhibitory and excitatory neurons, which form sophisticated microcircuits for processing and transmitting sensory information. Despite rapid progress in understanding the function of distinct neuronal populations, the parameters of connectivity that are required for the function of these microcircuits remain unknown. Recent studies found that two most common inhibitory interneurons, parvalbumin- (PV) and somatostatin-(SST) positive interneurons control sound-evoked responses, temporal adaptation and network dynamics in the auditory cortex (AC). These studies can inform our understanding of parameters for the connectivity of excitatory-inhibitory cortical circuits. Specifically, we asked whether a common microcircuit can account for the disparate effects found in studies by different groups. By starting with a cortical rate model, we find that a simple current-compensating mechanism accounts for the experimental findings from multiple groups. They key mechanisms are two-fold. First, PVs compensate for reduced SST activity when thalamic inputs are strong with less compensation when thalamic inputs are weak. Second, SSTs are generally disinhibited by reduced PV activity regardless of thalamic input strength. These roles are augmented by plastic synapses. These roles reproduce the differential effects of PVs and SSTs in stimulus-specific adaptation, forward suppression and tuning-curve adaptation, as well as the influence of PVs on feedforward functional connectivity in the circuit. This circuit exhibits a balance of inhibitory and excitatory currents that persists on stimulation. This approach brings together multiple findings from different laboratories and identifies a circuit that can be used in future studies of upstream and downstream sensory processing.
Highlights
Detecting sudden changes in the acoustic environment and extracting relevant acoustic features from noise are important computations for auditory navigation and scene analysis
The mammalian auditory cortex is composed of multiple types of inhibitory and excitatory neurons, which form sophisticated microcircuits for processing and transmitting sensory information
Distinct inhibitory neuron subtypes play distinct functions in auditory processing, but it remains unknown what simple set of underlying mechanisms is responsible for inhibitory cortical function
Summary
Detecting sudden changes in the acoustic environment and extracting relevant acoustic features from noise are important computations for auditory navigation and scene analysis. Neurons in AC exhibit adaptation to repeated tones, which may be selective for an overrepresented stimulus, such as in stimulus-specific adaptation, or SSA [1,2] They exhibit forward suppression, in which a preceding stimulus masker tone drives a decrease in responses to the subsequent target tone [3,4]. Recent studies have identified the differential involvement of two distinct major classes of inhibitory neurons, parvalbumin-positive (PV) and somatostatin-positive (SST) neurons in these temporal paradigms These neurons differ morphologically and physiologically [5,6], and recent studies found that they play differential functions in auditory processing. PVs and SSTs play distinct roles in adaptation to repeated tones along the frequency response function of the target neuron [7]. We tested whether these results can be accounted for by the same set of mechanisms
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