Abstract
Receptive fields of sensory neurons are considered to be dynamic and depend on the stimulus history. In the auditory system, evidence of dynamic frequency-receptive fields has been found following stimulus-specific adaptation (SSA). However, the underlying mechanism and circuitry of SSA have not been fully elucidated. Here, we studied how frequency-receptive fields of neurons in rat inferior colliculus (IC) changed when exposed to a biased tone sequence. Pure tone with one specific frequency (adaptor) was presented markedly more often than others. The adapted tuning was compared with the original tuning measured with an unbiased sequence. We found inhomogeneous changes in frequency tuning in IC, exhibiting a center-surround pattern with respect to the neuron's best frequency. Central adaptors elicited strong suppressive and repulsive changes while flank adaptors induced facilitative and attractive changes. Moreover, we proposed a two-layer model of the underlying network, which not only reproduced the adaptive changes in the receptive fields but also predicted novelty responses to oddball sequences. These results suggest that frequency-specific adaptation in auditory midbrain can be accounted for by an adapted frequency channel and its lateral spreading of adaptation, which shed light on the organization of the underlying circuitry.
Highlights
From the perspective of sensory coding, neurons encode information more effectively by adjusting their dynamic range and magnitude of sensitivity with the ongoing stimulus stream (Müller et al, 1999; Brenner et al, 2000; Dragoi et al, 2002; Krekelberg et al, 2006; Sharpee et al, 2006; Gutnisky and Dragoi, 2008; Zhao and Zhaoping, 2011; Benucci et al, 2013)
The absolute value of the adaptor position was smaller than 1 if the adaptor was inside the receptive fields (RFs), otherwise it was larger than 1.When the adaptor position was at a slightly lower frequency than the cell’s original best frequency (BF), the preferred frequency shifted to the higher frequencies, away from the adaptor (Figure 1C, left)
When the adaptor position was slightly higher than the original BF, the preferred frequency shifted to the lower frequency (Figure 1C, right)
Summary
From the perspective of sensory coding, neurons encode information more effectively by adjusting their dynamic range and magnitude of sensitivity with the ongoing stimulus stream (Müller et al, 1999; Brenner et al, 2000; Dragoi et al, 2002; Krekelberg et al, 2006; Sharpee et al, 2006; Gutnisky and Dragoi, 2008; Zhao and Zhaoping, 2011; Benucci et al, 2013). Stimulus-specific adaptation (SSA), in which rare stimuli elicit stronger responses than common ones, was first observed by presenting an oddball stimulus sequence with an unbalanced presentation probability of a rare and a common stimulus (Ulanovsky et al, 2003). This phenomenon was found in both cortical (Ulanovsky et al, 2003, 2004) and sub-cortical. If that is the case, the weakened response to common stimuli will not be limited to the particular stimuli presented but will occur with tones at neighboring frequencies
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