Nonuniform impacts of forward suppression on neural responses to preferred stimuli and nonpreferred stimuli in the rat auditory cortex

Abstract

In natural conditions, human and animals need to extract target sound information from noisy acoustic environments for communication and survival. However, how the contextual environmental sounds impact the tuning of central auditory neurons to target sound source azimuth over a wide range of sound levels is not fully understood. Here, we determined the azimuth-level response areas (ALRAs) of rat auditory cortex neurons by recording their responses to probe tones varying with levels and sound source azimuths under both quiet (probe alone) and forward masking conditions (preceding noise + probe). In quiet, cortical neurons responded stronger to their preferred stimuli than to their nonpreferred stimuli. In forward masking conditions, an effective preceding noise reduced the extents of the ALRAs and suppressed the neural responses across the ALRAs by decreasing the response strength and lengthening the first-spike latency. The forward suppressive effect on neural response strength was increased with increasing masker level and decreased with prolonging the time interval between masker and probe. For a portion of cortical neurons studied, the effects of forward suppression on the response strength to preferred stimuli was weaker than those to nonpreferred stimuli, and the recovery from forward suppression of the response strength to preferred stimuli was earlier than that to nonpreferred stimuli. We suggest that this nonuniform forward suppression of neural responses to preferred stimuli and to nonpreferred stimuli is important for cortical neurons to maintain their relative stable preferences for target sound source azimuth and level in noisy acoustic environments.

Chronic Unilateral Hearing Loss Disrupts Neural Tuning to Sound-Source Azimuth in the Rat Primary Auditory Cortex

“…In the present study, the azimuth functions of AI neurons obtained from two control groups demonstrated that more than half of the neurons in the rat AI preferred sound stimuli from the contralateral azimuth in the horizontal plane. This is consistent with the findings shown in previous studies regarding the spatial representation of rat AI neurons measured by spike counts (Yao et al, 2013; Gao et al, 2018) and excitatory postsynaptic potentials (Chadderton et al, 2009). Studies using interaural level differences to mimic the changes of spatial azimuth also demonstrated that most tested neurons in the rat AI preferred acoustic stimuli from contralateral horizontal positions (Kelly and Sally, 1988).…”

“…Most of the neurons in AI preferred sound stimuli from the contralateral field, and only a small proportion of neurons preferred the sound stimuli from midline or ipsilateral field. This has been demonstrated in cats (Imig et al, 1990; Rajan et al, 1990; Barone et al, 1996; Eggermont and Mossop, 1998), rats (Yao et al, 2013; Gao et al, 2018), and monkeys (Woods et al, 2006). Studies also showed that many azimuth-sensitive neurons in the AI of adult cats determined in binaural conditions immediately became insensitive to sound source azimuth when determined with one ear plugged (Samson et al, 1994), demonstrating the importance of normal binaural input in the spatial sensitivity of AI neurons.…”

“…In the present study, we investigated whether identical UCHL manipulation carried out in young rats and adult rats produces the same outcome in the neural representation of spatial azimuth in the rat AI. Because previous studies have demonstrated a dominant preference of AI neurons to stimuli from the contralateral auditory space (Imig et al, 1990; Rajan et al, 1990; Barone et al, 1996; Eggermont and Mossop, 1998; Woods et al, 2006; Gao et al, 2018; Yao and Sanes, 2018), we here focused on studying the impacts of postnatal UCHL on the neural tuning to sound source azimuth in the AI contralateral the operated ear. We found that chronic UCHL carried out at both young and adult ages altered the azimuth preference, degraded the azimuth selectivity and sensitivity of AI neurons.…”

Unilateral Conductive Hearing Loss Disrupts the Developmental Refinement of Binaural Processing in the Rat Primary Auditory Cortex

“…Our data show that majority of AI neurons preferred ILDs favoring contralateral spatial azimuth in both the adult and developing rats (Figure 8). Studies in the adult animals in a variety of species have demonstrated the dominant preference of AI neurons to contralateral spatial locations, e.g., in cats (Irvine et al, 1996;Zhang et al, 2004), bats (Razak, 2011), monkeys (Zhou and Wang, 2012;Lui et al, 2015), rats (Yao et al, 2013;Gao et al, 2018;Wang et al, 2019), and mice (Panniello et al, 2018). The results in the immature rats suggest that the dominant contralateral preference of AI neurons is already present immediately after the onset of hearing and is adult-like.…”

“…Lesion or inactivation of AI leads to sound localization deficits (Malhotra and Lomber, 2007;Nodal et al, 2010). AI neurons have been shown to be sensitivity to sound-source azimuth in cats (Samson et al, 1994), monkeys (Woods et al, 2006), bats (Razak, 2011), ferrets (Wood et al, 2019), and rats (Yao et al, 2013;Gao et al, 2018;Wang et al, 2019). The spatial sensitivity of AI neurons to sound-source azimuth largely depends on binaural processing.…”