Abstract
Frequency modulations occur in many natural sounds, including vocalizations. The neuronal response to frequency modulated (FM) stimuli has been studied extensively in different brain areas, with an emphasis on the auditory cortex and the central nucleus of the inferior colliculus. Here, we measured the responses to FM sweeps in whole-cell recordings from neurons in the dorsal cortex of the mouse inferior colliculus. Both up- and downward logarithmic FM sweeps were presented at two different speeds to both the ipsi- and the contralateral ear. Based on the number of action potentials that were fired, between 10 and 24% of cells were selective for rate or direction of the FM sweeps. A somewhat lower percentage of cells, 6–21%, showed selectivity based on EPSP size. To study the mechanisms underlying the generation of FM selectivity, we compared FM responses with responses to simple tones in the same cells. We found that if pairs of neurons responded in a similar way to simple tones, they generally also responded in a similar way to FM sweeps. Further evidence that FM selectivity can be generated within the dorsal cortex was obtained by reconstructing FM sweeps from the response to simple tones using three different models. In about half of the direction selective neurons the selectivity was generated by spectrally asymmetric synaptic inhibition. In addition, evidence for direction selectivity based on the timing of excitatory responses was also obtained in some cells. No clear evidence for the local generation of rate selectivity was obtained. We conclude that FM direction selectivity can be generated within the dorsal cortex of the mouse inferior colliculus by multiple mechanisms.
Highlights
Most natural sounds vary in the frequency domain
To explore if Frequency modulation (FM) selectivity can be generated in the dorsal cortex of the inferior colliculus, we reconstructed responses to FM sweeps from frequency response areas (FRAs) and we develop quantitative measures to quantify how well the reconstruction match the recorded responses
Our results show that neurons in the dorsal cortex of the mouse inferior colliculus can respond selectively to the direction or rate of FM sweeps
Summary
Most natural sounds vary in the frequency domain. Frequency modulation (FM) is an important component of animal communication, including speech (Stein, 1968; Ryan, 1983; Kanwal et al, 1994; Holy and Guo, 2005; Zeng et al, 2005). The mechanisms generating FM selectivity in the central nucleus of the inferior colliculus have received a lot of attention These studies have demonstrated that spectrally asymmetric synaptic inhibition plays an important role in creating FM direction selectivity within the inferior colliculus (reviewed in Fuzessery et al, 2011; Pollak et al, 2011). In these cells, for the preferred sweep direction excitation precedes inhibition, whereas for the other direction inhibition coincides with excitation. It is still debated whether this mechanism can entirely explain FM direction selectivity within the inferior colliculus, or whether there is an additional role for upstream processing or the timing of excitatory inputs (Suga, 1965; Clopton and Winfield, 1974; Poon et al, 1992; Felsheim and Ostwald, 1996; Gittelman et al, 2009; Williams and Fuzessery, 2011; Kuo and Wu, 2012)
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