Abstract
Hierarchical processing of sensory information requires interaction at multiple levels along the peripheral to central pathway. Recent evidence suggests that interaction between driving and modulating components can shape both top down and bottom up processing of sensory information. Here we show that a component inherited from extrinsic sources combines with local components to code sound intensity. By applying high concentrations of divalent cations to neurons in the nucleus of the inferior colliculus in the auditory midbrain, we show that as sound intensity increases, the source of synaptic efficacy changes from inherited inputs to local circuits. In neurons with a wide dynamic range response to intensity, inherited inputs increase firing rates at low sound intensities but saturate at mid-to-high intensities. Local circuits activate at high sound intensities and widen dynamic range by continuously increasing their output gain with intensity. Inherited inputs are necessary and sufficient to evoke tuned responses, however local circuits change peak output. Push–pull driving inhibition and excitation create net excitatory drive to intensity-variant neurons and tune neurons to intensity. Our results reveal that dynamic range and tuning re-emerge in the auditory midbrain through local circuits that are themselves variable or tuned.
Highlights
Sensory systems use distinct coding strategies to represent complex stimuli
We isolated responses to extrinsic inputs from those evoked by local circuits by blocking polysynaptic activity locally in the inferior colliculus (IC) by applying ACSF containing a raised concentration of Ca2+ and Mg2+
For IC neurons, this concentration is achieved by raising Ca2+ and Mg2+ 2.5-fold (2.5 high concentration of divalent cations (HiDi); Sivaramakrishnan et al, 2013)
Summary
Information contained within the intensity of a sensory stimulus, for example, is coded in different ways to extract multiple features of the input. Intensity-variant codes provide information about the context of a sensory stimulus, such as previous history or regional interaction (Albright and Stoner, 2002; Bartlett and Wang, 2005). Variant and tuned intensity codes are found at multiple central levels of the auditory system (Sivaramakrishnan et al, 2004; Billimoria et al, 2008; Sadagopan and Wang, 2008; Barbour, 2011) and lie at the extremes of the dynamic range spectrum of sound intensity. From the standpoint of a population code, the dynamic range continuum allows for plasticity in information transfer about sound level. Level variance changes to level tuning, for example, following conditioning (Polley et al, 2004) or negative gain control (Sivaramakrishnan et al, 2004), and level codes and receptive fields adapt to changing sound stimuli, shifting their operating points toward preferred sound levels (Kvale and Schreiner, 2004; Dean et al, 2005)
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