Abstract
Auditory neurons in bats that use frequency modulated (FM) sweeps for echolocation are selective for the behaviorally-relevant rates and direction of frequency change. Such selectivity arises through spectrotemporal interactions between excitatory and inhibitory components of the receptive field. In the pallid bat auditory system, the relationship between FM sweep direction/rate selectivity and spectral and temporal properties of sideband inhibition have been characterized. Of note is the temporal asymmetry in sideband inhibition, with low-frequency inhibition (LFI) exhibiting faster arrival times compared to high-frequency inhibition (HFI). Using the two-tone inhibition over time (TTI) stimulus paradigm, this study investigated the interactions between two sound parameters in shaping sideband inhibition: intensity and time. Specifically, the impact of changing relative intensities of the excitatory and inhibitory tones on arrival time of inhibition was studied. Using this stimulation paradigm, single unit data from the auditory cortex of pentobarbital-anesthetized cortex show that the threshold for LFI is on average ~8 dB lower than HFI. For equal intensity tones near threshold, LFI is stronger than HFI. When the inhibitory tone intensity is increased further from threshold, the strength asymmetry decreased. The temporal asymmetry in LFI vs. HFI arrival time is strongest when the excitatory and inhibitory tones are of equal intensities or if excitatory tone is louder. As inhibitory tone intensity is increased, temporal asymmetry decreased suggesting that the relative magnitude of excitatory and inhibitory inputs shape arrival time of inhibition and FM sweep rate and direction selectivity. Given that most FM bats use downward sweeps as echolocation calls, a similar asymmetry in threshold and strength of LFI vs. HFI may be a general adaptation to enhance direction selectivity while maintaining sweep-rate selective responses to downward sweeps.
Highlights
Bats of the suborder, microchiroptera, can be broadly classified as constant frequency-frequency modulation (CF-FM) or frequency modulation (FM) bats based on their echolocation calls (Jones and Teeling, 2006)
When the low-frequency inhibition (LFI) tone was presented at an intensity 10 dB lower than the excitatory tone (I-E = −10 dB), the response of the neuron decreased relative to the control response, but did not meet the 50% criterion to determine arrival time
When the intensity of the LFI tone was increased by 5 dB, while maintaining the excitatory tone intensity (I-E = −5 dB), the response of the neuron decreased below 50% of control response when the delay was ∼1.5 ms
Summary
Microchiroptera, can be broadly classified as constant frequency-frequency modulation (CF-FM) or frequency modulation (FM) bats based on their echolocation calls (Jones and Teeling, 2006). Beginning with studies by Suga (1965), one conceptual framework to study mechanisms underlying FM sweep rate and direction selectivity is based on asymmetries in sideband inhibition Auditory neurons, like those in the visual and somatosensory systems, exhibit excitatory and inhibitory components in the receptive field (Calford and Semple, 1995; Brosch and Schreiner, 1997; Gordon and O’Neill, 1998; Sutter et al, 1999; Faure et al, 2003; Wehr and Zador, 2003; Razak and Fuzessery, 2006; Wu et al, 2008; Sadagopan and Wang, 2010; Kuo and Wu, 2012). In its simplest form, the asymmetry hypothesis suggests that absent inhibition on one side of the tuning curve will cause a neuron to be sweep direction selective
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