Amplitude modulation (AM) is an important feature in human speech, music, animal vocalization and environmental sounds (Shannon et al. 1995, Hoglen et al. 2018, Joris et al. 2004, Miller and Hauser 2004), which exhibit periodic and aperiodic temporal cues as the amplitude envelope changes. Deficiencies in processing AM temporal cues impair sound perception in older and hearing-impaired listeners, even when audibility is accounted for (Jorgensen and Dau 2011, Fullgrabe et al. 2015).

In the auditory nerve and the cochlear nuclei, periodic AM is represented primarily by synchronized spiking that is phase-locked to the AM frequency (AMF), while mean firing rate does not change significantly (Joris et al. 1994, Joris et al. 2004, Wiegriebe and Meddis 2004). By contrast, neurons in the inferior colliculus (IC) respond to changes in AMF by altering their phase-locked response as well as their firing rates (Krishna and Semple 2000, Nelson and Carney 2007, Rabang et al. 2012, Herrmann et al. 2017, Parthasarathy et al. 2019). IC firing rates change as a function of modulation frequency, and the shapes of modulation frequency tuning curves (band-pass, band-reject, low-pass, etc.) are preserved across species and anesthetized versus awake preparations (Shaddock Palombi et al. 2001, Rabang et al. 2012, Ter-Mikaelian et al. 2007, Nelson and Carney 2007). Both rate and synchrony of IC neurons decline with decreasing AM depth (Nelson and Carney 2007), and these declines correlate with reduced perceptual detection (Henry et al. 2016.). With aging, auditory evoked potential responses and behavioral capabilities for AM depth detection and AMF discrimination decline (Suta et al. 2011, Parthasarathy and Bartlett 2011, Ouda et al. 2015, Lai et al. 2022). This is likely due to changes in the both the IC neurons and local networks as well as changes in the inputs to the IC neurons. Analyses at multiple levels of the central auditory pathway, including the IC, have shown significant synaptic and metabolic changes in older individuals (Helfert et al. 1999, Holt et al. 2006, Tadros et al. 2007, Syka 2020). Such changes are most evident in inhibitory GABAergic and glycinergic synapses, which are rich in the IC (Merchan et al. 2005), with GABAergic synapse and cell loss being the most prominent (Caspary et al. 1990, Caspary et al. 1999, Syka et al. 2002, Caspary et al. 2008, Pal et al. 2019, Koehler et al. 2023). Despite this, the effects of reduced inhibition on frequency and temporal processing of sounds with clear acoustic cues (i.e. tone in quiet or 100% modulation depth) have been fairly limited. In bats and chinchillas, blockade of GABAA inhibition does not change the phase-locking rate of bat IC central nucleus neurons to AM stimuli (Burger and Pollak 1998, Caspary, Palombi, and Hughes 2002). These reductions in inhibition are thought to partially compensate for weaker cochlear and auditory nerve excitation, resulting in an amplification of auditory inputs often known as enhanced central gain (Chambers et al. 2016, Parthasarathy et al. 2019, Johannesen et al. 2021) and reduced latencies (Simon et al. 2004). Such compensation often disrupts subtle spectrotemporal processing, particularly when a target sound has weaker acoustic features (Kommajosyula et al. 2019, 2021), such as being embedded in noise or having small modulation depth. Notably, few IC studies have looked at the effect of reduced AM depth with aging. Walton and colleagues (Walton et al. 1998, 2002, Walton 2010) have investigated the aging IC in mice, and they found that older mice exhibited behavioral deficits along with a higher firing rate and lower vector strength compared to younger mice.

One way to dissociate the IC inputs from the IC outputs is to compare local field potentials (LFPs) and spiking IC responses recorded simultaneously. LFPs provide an aggregate measure of synaptic activity and are strongly diminished by blocking excitatory postsynaptic receptors in IC (Bullock, 1997, Buzsaki et al. 2012, Logothetis et al. 2001, Logothetis and Wandell 2004, Patel et al. 2012). By measuring both LFPs and spiking activities at a given recording site, it is possible to determine whether LFP and spiking neurometric thresholds (rate or synchrony) are comparable. Furthermore, one can assess the extent to which IC outputs relay their inputs or whether they are able to compensate for weaker or less coherent LFP (synaptic) inputs, given that aging and hearing loss both produce compensation in the IC dominated wave 5 ABR wave (Johannesen et al. 2021, Lai et al. 2017, Parthasarathy and Bartlett 2012, Parthasarathy et al. 2014)

In this study, we recorded from Young and Aged F344 rats, using LFPs, phase-locking, and firing rates of IC neurons to evaluate the temporal processing of inputs to and outputs from IC neurons as a function of modulation depth and age