Frequency tuning of synaptic inhibition underlying duration-tuned neurons in the mammalian inferior colliculus

Abstract

Inhibition plays an important role in creating the temporal response properties of duration-tuned neurons (DTNs) in the mammalian inferior colliculus (IC). Neurophysiological and computational studies indicate that duration selectivity in the IC is created through the convergence of excitatory and inhibitory synaptic inputs offset in time. We used paired-tone stimulation and extracellular recording to measure the frequency tuning of the inhibition acting on DTNs in the IC of the big brown bat (). We stimulated DTNs with pairs of tones differing in duration, onset time, and frequency. The onset time of a short, best-duration (BD), probe tone set to the best excitatory frequency (BEF) was varied relative to the onset of a longer-duration, nonexcitatory (NE) tone whose frequency was varied. When the NE tone frequency was near or within the cell's excitatory bandwidth (eBW), BD tone-evoked spikes were suppressed by an onset-evoked inhibition. The onset of the spike suppression was independent of stimulus frequency, but both the offset and duration of the suppression decreased as the NE tone frequency departed from the BEF. We measured the inhibitory frequency response area, best inhibitory frequency (BIF), and inhibitory bandwidth (iBW) of each cell. We found that the BIF closely matched the BEF, but the iBW was broader and usually overlapped the eBW measured from the same cell. These data suggest that temporal selectivity of midbrain DTNs is created and preserved by having cells receive an onset-evoked, constant-latency, broadband inhibition that largely overlaps the cell's excitatory receptive field. We conclude by discussing possible neural sources of the inhibition. Duration-tuned neurons (DTNs) arise from temporally offset excitatory and inhibitory synaptic inputs. We used single-unit recording and paired-tone stimulation to measure the spectral tuning of the inhibitory inputs to DTNs. The onset of inhibition was independent of stimulus frequency; the offset and duration of inhibition systematically decreased as the stimulus departed from the cell's best excitatory frequency. Best inhibitory frequencies matched best excitatory frequencies; however, inhibitory bandwidths were more broadly tuned than excitatory bandwidths.

Effect of sound pressure level on contralateral inhibition underlying duration-tuned neurons in the mammalian inferior colliculus

“…It is also possible that the strength of excitation could change relative to the strength of inhibition as stimulus amplitude increases. If the strength of excitation increased faster than that of inhibition, FSLs would be expected to decrease at louder SPLs as is the case for most central auditory neurons (Heil 2004;Klug et al 2000;Mörchen et al 1978;Rose et al 1963;Tan et al 2008). If the strength of inhibition increased faster than that of excitation, FSLs should lengthen and the cell should demonstrate a paradoxical latency shift (PLS) at increasing SPLs (Covey et al 1996;Galazyuk et al 2005;Galazyuk and Feng 2001;Hechavarría et al 2011;Hechavarría and Kössl 2014;Klug et al 2000;Macías et al 2016;Sullivan 1982aSullivan , 1982b.…”

Absence of the Fragile X messenger ribonucleoprotein alters response patterns to sounds in the auditory midbrain

“…In the IC, offset activity may be evoked by excitatory synaptic inputs occurring after sound termination or by inhibitory rebound activity (Kasai et al, 2012). The temporal pattern of the excitatory and inhibitory responses to the beginning and the end of a sound stimulus also determines the selectivity of neurons to the duration of a sound (Ono and Oliver, 2014;Valdizón-Rodríguez and Faure, 2017;Valdizón-Rodríguez et al, 2019). What are the possible underlying cellular mechanisms associated with this enhanced offset activity in Fmr1 -/-neurons?…”

Testing inferior colliculus neurons for selectivity to the rate or duration of frequency modulated sweeps

“…Detailed explanations of animal care and institutional approval, surgical preparation and anaesthesia, stimulus generation, and neural recording procedures have been published [21,22].…”