Behavioral Plasticity of Audiovisual Perception: Rapid Recalibration of Temporal Sensitivity but Not Perceptual Binding Following Adult-Onset Hearing Loss

Abstract

The ability to accurately integrate or bind stimuli from more than one sensory modality is highly dependent on the features of the stimuli, such as their intensity and relative timing. Previous studies have demonstrated that the ability to perceptually bind stimuli is impaired in various clinical conditions such as autism, dyslexia, schizophrenia, as well as aging. However, it remains unknown if adult-onset hearing loss, separate from aging, influences audiovisual temporal acuity. In the present study, rats were trained using appetitive operant conditioning to perform an audiovisual temporal order judgment (TOJ) task or synchrony judgment (SJ) task in order to investigate the nature and extent that audiovisual temporal acuity is affected by adult-onset hearing loss, with a specific focus on the time-course of perceptual changes following loud noise exposure. In our first series of experiments, we found that audiovisual temporal acuity in normal-hearing rats was influenced by sound intensity, such that when a quieter sound was presented, the rats were biased to perceive the audiovisual stimuli as asynchronous (SJ task), or as though the visual stimulus was presented first (TOJ task). Psychophysical testing demonstrated that noise-induced hearing loss did not alter the rats’ temporal sensitivity 2–3 weeks post-noise exposure, despite rats showing an initial difficulty in differentiating the temporal order of audiovisual stimuli. Furthermore, consistent with normal-hearing rats, the timing at which the stimuli were perceived as simultaneous (i.e., the point of subjective simultaneity, PSS) remained sensitive to sound intensity following hearing loss. Contrary to the TOJ task, hearing loss resulted in persistent impairments in asynchrony detection during the SJ task, such that a greater proportion of trials were now perceived as synchronous. Moreover, psychophysical testing found that noise-exposed rats had altered audiovisual synchrony perception, consistent with impaired audiovisual perceptual binding (e.g., an increase in the temporal window of integration on the right side of simultaneity; right temporal binding window (TBW)). Ultimately, our collective results show for the first time that adult-onset hearing loss leads to behavioral plasticity of audiovisual perception, characterized by a rapid recalibration of temporal sensitivity but a persistent impairment in the perceptual binding of audiovisual stimuli.

Compensatory Plasticity in the Lateral Extrastriate Visual Cortex Preserves Audiovisual Temporal Processing following Adult-Onset Hearing Loss

“…Consistent with human testing, a psychophysical profile was generated for each rat by plotting straight lines between each of the neighboring SOAs and the associated slope and intercept values were calculated [26]. Using these values, the point of subjective simultaneity (PSS) and just noticeable difference (JND) was calculated for each of the test sessions [24, 25, 27]. For each of the SJ test sessions, performance for all 5 SOAs was measured as the proportion of trials in which the rat perceived the stimuli as synchronous (i.e., responded to the left feeder trough, Figure 1(a)).…”

“…Of the few reports available, however, it appears that audiovisual synchrony perception is largely preserved in hearing-impaired subjects [21–23], provided that potential confounding factors, such as aging, are addressed. Moreover, we recently reported that adult rats with a moderate hearing loss experienced a rapid recalibration of their ability to accurately judge the order of audiovisual stimuli, with temporal perception being restored two weeks following the loud noise exposure [24]. This inconsistency between the extent of crossmodal plasticity reported previously and the apparent lack of behavioral consequences raises an important question: how is the brain able to maintain (or re-establish) temporally precise audiovisual integration and perception in the presence of extensive sensory reorganization in the cortical regions thought to subserve such behavioral tasks?…”

Approaches to Understanding Multisensory Dysfunction in Autism Spectrum Disorder

“…SJ and TOJ tasks : [Schormans & Allman, 2018; Schormans, Scott, et al, 2017; Schormans, Typlt, & Allman, 2017]…”

“…In the awake, behaving rat, Hirokawa and colleagues used pharmacology to transiently disrupt and identify a border region between the primary visual and auditory cortices, known as the lateral part of V2 or V2L, that is critical for audiovisual processing in rats [Hirokawa et al, 2008]. Allman and colleagues recently investigated the role of V2L in multisensory temporal processing [Schormans & Allman, 2018; Schormans, Scott, et al, 2017]. Remarkably, rats are capable of performing classic psychophysical simultaneity judgment (SJ) and temporal order judgment (TOJ) tasks [Schormans, Scott, et al, 2017], generating TBWs that appear to be similar to those found in the human population [Wallace & Stevenson, 2014].…”

“…To this point, studies are already using very similar psychophysical experiments as observed in humans to demonstrate multisensory temporal processing and temporal binding windows (TBWs) in rats and have identified the neural structures needed for this multisensory behavior [Schormans & Allman, 2018; Schormans, Scott, et al, 2017; Schormans, Typlt, & Allman, 2017]. Therefore, can mouse studies be refined to evaluate multisensory temporal processing, including temporal binding windows, and would these tasks implicate brain regions (i.e.…”