Recovery cycle times of inferior colliculus neurons in the awake bat measured with spike counts and latencies

Abstract

Neural responses in the mammalian auditory midbrain (inferior colliculus; IC) arise from complex interactions of synaptic excitation, inhibition, and intrinsic properties of the cell. Temporally selective duration-tuned neurons (DTNs) in the IC are hypothesized to arise through the convergence of excitatory and inhibitory synaptic inputs offset in time. Synaptic inhibition can be inferred from extracellular recordings by presenting pairs of pulses (paired tone stimulation) and comparing the evoked responses of the cell to each pulse. We obtained single unit recordings from the IC of the awake big brown bat (Eptesicus fuscus) and used paired tone stimulation to measure the recovery cycle times of DTNs and non-temporally selective auditory neurons. By systematically varying the interpulse interval (IPI) of the paired tone stimulus, we determined the minimum IPI required for a neuron's spike count or its spike latency (first- or last-spike latency) in response to the second tone to recover to within ≥50% of the cell's baseline count or to within 1 SD of it's baseline latency in response to the first tone. Recovery times of shortpass DTNs were significantly shorter than those of bandpass DTNs, and recovery times of bandpass DTNs were longer than allpass neurons not selective for stimulus duration. Recovery times measured with spike counts were positively correlated with those measured with spike latencies. Recovery times were also correlated with first-spike latency (FSL). These findings, combined with previous studies on duration tuning in the IC, suggest that persistent inhibition is a defining characteristic of DTNs. Herein, we discuss measuring recovery times of neurons with spike counts and latencies. We also highlight how persistent inhibition could determine neural recovery times and serve as a potential mechanism underlying the precedence effect in humans. Finally, we explore implications of recovery times for DTNs in the context of bat hearing and echolocation.

Organization and trade-off of spectro-temporal tuning properties of duration-tuned neurons in the mammalian inferior colliculus

“…As expected from previous reports (e.g., Pinheiro et al 1991;Haplea et al 1994;Faure et al 2003;Jen and Wu 2006;Sayegh et al 2012), DTNs exhibited a robust tonotopic organization and had neural thresholds that increased with recording electrode depth in the IC and that covered the dynamic range of hearing (Figs. 3-4).…”

“…First, we noted the stimulus value evoking the peak spike count and then found the lowest and highest stimulus frequencies or durations where the function dropped to Յ50% of the peak thus delimiting the lower and upper cut-offs of the 50% eFBW and 50% eDBW. Cut-offs were computed with two complementary methods (see Sayegh et al 2012, for use of a similar technique). The inside-out method started at the peak of a tuning function and moved outward, toward the minimum and maximum stimulus values along the abscissa, noting the first data points where the function decreased to Յ50% of the peak.…”

“…To date, research on auditory DTNs has focused primarily on the neural mechanisms that create their temporally selective responses Ehrlich et al 1997;Fuzessery and Hall 1999;Hooper et al 2002;Faure et al 2003;Jen and Wu 2006;Aubie et al 2009Aubie et al , 2012Sayegh et al 2012Sayegh et al , 2014 and on the stability (tolerance) of duration tuning with changes in signal amplitude (Zhou and Jen 2001;Mora and Kössl 2004;Fremouw et al 2005). We know that duration tuning is disrupted or abolished by blocking neural inhibition in the IC, which also suggests that duration tuning originates there Faure et al 2003;Leary et al 2008).…”

High concentrations of divalent cations isolate monosynaptic inputs from local circuits in the auditory midbrain

“…We measured an average control FSL of 15.34 ± 6.15 ms SD ( n = 88). The large SD of our population data reflects the wide distribution of FSLs (~5–30 ms), which has been previously reported in the unanesthetized IC (Sivaramakrishnan et al, 2004; Sanchez et al, 2007; Sayegh et al, 2012). If this wide range of FSLs reflects a range of monosynaptic, disynaptic, or polysynaptic inputs then, by parallels with brain slice recordings, a shortening of FSLs with increases in sound intensity should imply that a polysynaptic pathway within the IC was included in determining the FSL for a given neuron.…”

Local inhibition of GABA affects precedence effect in the inferior colliculus

“…The existence of precedence effect is therefore a prerequisite for the faithful sound localization in natural reverberant environments[12164950]. …”