A temporal integration mechanism enhances frequency selectivity of broadband inputs to inferior colliculus

Abstract

Accurately resolving frequency components in sounds is essential for sound recognition, yet there is little direct evidence for how frequency selectivity is preserved or newly created across auditory structures. We demonstrate that prepotentials (PPs) with physiological properties resembling presynaptic potentials from broadly tuned brainstem inputs can be recorded concurrently with postsynaptic action potentials in inferior colliculus (IC). These putative brainstem inputs (PBIs) are broadly tuned and exhibit delayed and spectrally interleaved excitation and inhibition not present in the simultaneously recorded IC neurons (ICNs). A sharpening of tuning is accomplished locally at the expense of spike-timing precision through nonlinear temporal integration of broadband inputs. A neuron model replicates the finding and demonstrates that temporal integration alone can degrade timing precision while enhancing frequency tuning through interference of spectrally in- and out-of-phase inputs. These findings suggest that, in contrast to current models that require local inhibition, frequency selectivity can be sharpened through temporal integration, thus supporting an alternative computational strategy to quickly refine frequency selectivity.

Frequency response areas of neurons in the mouse inferior colliculus. III. Time-domain responses: Constancy, dynamics, and precision in relation to spectral resolution, and perception in the time domain

“…Our results clearly showed that neurons of FRA classes I and III with phasic responses had both the smallest latency jitter and jitter variation compared with neurons of other temporal responses of the same FRA class and with neurons of FRA class II ( Fig 12 ). The average values of first spike latency jitter of 0.367 ms (class I) and 0.560 ms (class III) were very similar to jitter values < 1 ms found in the ICC of the mouse [ 81 ], rat [ 82 ], cat [ 47 ], guinea pig [ 39 ], and bat [ 83 , 84 ]. These values of latency jitter were in the range of 0.1–1 ms as found in the auditory nerve and auditory cortex [ 65 ].…”

“…In conclusion, the above-mentioned mapping data about neuronal response properties in the ICC support the notion that auditory brainstem input is subject to some transformation in the ICC with enhancement of spectral resolution by degradation of timing precision and enhancement of timing precision by degradation of spectral resolution [ 46 , 47 ]. Neurons of FRA classes II and III appear to be representatives of such transformations, also with regard to transformation of auditory coding, by various aspects of neuronal responses, to certain local conditions in the ICC space [ 5 , 32 , 45 ].…”

“…Besides tone-response patterns, tone-response latencies could vary within the FRAs of the neurons. Latencies of guinea pig, rat, bat, and cat ICC neurons with temporal response patterns such as phasic , tonic , phasic-tonic , pauser (and variants thereof) have been reported to be, on average, in a range of up to about 15 ms [ 39 , 47 , 69 , 78 , 79 ], in the mouse ICC up to about 20 ms [ 21 , 80 , 81 ], which was the value we used here to separate short-latency from long-latency responses (latencies > 20 ms). Average latencies of the short-latency response patterns ( phasic , tonic , phasic-tonic , pauser ) and of the neurons in the three classes of FRAs did not differ significantly (Tables 1 and S1A ).…”

“…The hypothesis is that ICC neurons specialize in spectral or temporal coding as has been suggested using a different experimental approach, i.e. recordings of spectrotemporal receptive fields with frequency/amplitude-modulated sounds in the ICC of the cat [ 46 , 47 ]. Also, the kind and degree of specialization may bear reference to their location in the ICC.…”

Developmentally Regulated Rebound Depolarization Enhances Spike Timing Precision in Auditory Midbrain Neurons

“…IC neurons are critically involved in processing important temporal features of sounds (Wenstrup et al, 2012 ; Chen et al, 2019 ; Yang et al, 2020 ). One striking biophysical property of IC neurons is rebound depolarization (Sun and Wu, 2008a ; Kasai et al, 2012 ; Chandrasekaran et al, 2013 ; Ayala and Malmierca, 2018 ).…”