Abstract
We studied the columnar and layer-specific response properties of neurons in the primary auditory cortex (A1) of six (four females, two males) anesthetized free-tailed bats, Tadarida brasiliensis, in response to pure tones and down and upward frequency modulated (FM; 50 kHz bandwidth) sweeps. In addition, we calculated current source density (CSD) to test whether lateral intracortical projections facilitate neuronal activation in response to FM echoes containing spectrally distant frequencies from the excitatory frequency response area (FRA). Auditory responses to a set of stimuli changing in frequency and level were recorded along 64 penetrations in the left A1 of six free-tailed bats. FRA shapes were consistent across the cortical depth within a column and there were no obvious differences in tuning properties. Generally, response latencies were shorter (<10 ms) for cortical depths between 500 and 600 μm, which might correspond to thalamocortical input layers IIIb–IV. Most units showed a stronger response to downward FM sweeps, and direction selectivity did not vary across cortical depth. CSD profiles calculated in response to the CF showed a current sink located at depths between 500 and 600 μm. Frequencies lower than the frequency range eliciting a spike response failed to evoke any visible current sink. Frequencies higher than the frequency range producing a spike response evoked layer IV sinks at longer latencies that increased with spectral distance. These data support the hypothesis that a progressive downward relay of spectral information spreads along the tonotopic axis of A1 via lateral connections, contributing to the neural processing of FM down sweeps used in biosonar.
Highlights
Numerous physiological studies of the auditory cortex in bats have revealed remarkable specializations for processing species-specific echolocation signals as well as a high diversity of the size and arrangement of functional fields (Suga, 1984, 2012; Dear et al, 1993; O’Neill, 1995; Hoffmann et al, 2008; Kössl et al, 2014, 2015)
We found that the majority of neurons in the free-tailed bat A1 were preferentially sensitive to downward FM sweeps used in their biosonar, and FM sweep selectivity in the A1 is known to arise from local intracortical networks (Razak and Fuzessery, 2006), so we decided to exploit this property of the system to closely examine the laminar characteristics of selectivity to the direction of frequency modulated (FM) sweeps
Auditory responses were recorded along 64 penetrations in the left A1 of six anesthetized free-tailed bats (12, 11, 14, 12, 8 and 7 penetrations, respectively per bat), while presenting a set of stimuli changing in frequency and level
Summary
Numerous physiological studies of the auditory cortex in bats have revealed remarkable specializations for processing species-specific echolocation signals as well as a high diversity of the size and arrangement of functional fields (Suga, 1984, 2012; Dear et al, 1993; O’Neill, 1995; Hoffmann et al, 2008; Kössl et al, 2014, 2015). We found that the majority of neurons in the free-tailed bat A1 were preferentially sensitive to downward FM sweeps used in their biosonar, and FM sweep selectivity in the A1 is known to arise from local intracortical networks (Razak and Fuzessery, 2006), so we decided to exploit this property of the system to closely examine the laminar characteristics of selectivity to the direction of frequency modulated (FM) sweeps. FM direction selectivity arises through asymmetric inhibitory sidebands on the frequency response areas (FRAs; Suga, 1965a,b; Heil et al, 1992a,b; Fuzessery and Hall, 1996; Gordon and O’Neill, 1998; Razak and Fuzessery, 2002, 2006, 2008; Zhang et al, 2003) In those cases, lateral inhibition from frequencies below a neuron’s FRA can blunt responses to anything but downward FM sweeps. CSD enabled us to compare mean synaptic activity in response to different pure tones of changing frequency and FM sweeps of different directions
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