Past and present experience shifts audiovisual temporal perception in rats

Abstract

Our brains have a propensity to integrate closely-timed auditory and visual stimuli into a unified percept; a phenomenon that is highly malleable based on prior sensory experiences, and is known to be altered in clinical populations. While the neural correlates of audiovisual temporal perception have been investigated using neuroimaging and electroencephalography techniques in humans, animal research will be required to uncover the underlying cellular and molecular mechanisms. Prior to conducting such mechanistic studies, it is important to first confirm the translational potential of any prospective animal model. Thus, in the present study, we conducted a series of experiments to determine if rats show the hallmarks of audiovisual temporal perception observed in neurotypical humans, and whether the rat behavioral paradigms could reveal when they experienced perceptual disruptions akin to those observed in neurodevelopmental disorders. After training rats to perform a temporal order judgment (TOJ) or synchrony judgment (SJ) task, we found that the rats' perception was malleable based on their past and present sensory experiences. More specifically, passive exposure to asynchronous audiovisual stimulation in the minutes prior to behavioral testing caused the rats' perception to predictably shift in the direction of the leading stimulus; findings which represent the first time that this form of audiovisual perceptual malleability has been reported in non-human subjects. Furthermore, rats performing the TOJ task also showed evidence of rapid recalibration, in which their audiovisual temporal perception on the current trial was predictably influenced by the timing lag between the auditory and visual stimuli in the preceding trial. Finally, by manipulating either experimental testing parameters or altering the rats' neurochemistry with a systemic injection of MK-801, we showed that the TOJ and SJ tasks could identify when the rats had difficulty judging the timing of audiovisual stimuli. These findings confirm that the behavioral paradigms are indeed suitable for future testing of rats with perceptual disruptions in audiovisual processing. Overall, our collective results highlight that rats represent an excellent animal model to study the cellular and molecular mechanisms underlying the acuity and malleability of audiovisual temporal perception, as they showcase the perceptual hallmarks commonly observed in humans.

Keywords: audiovisual temporal perception; rapid recalibration; rat; synchrony judgment; temporal order judgment.

Figure 1

Passive sensory exposure shifted perception while sparing audiovisual temporal acuity in rats performing the TOJ task. (A) Schematic overview of the rat temporal order judgment (TOJ) task within the operant chamber (created with BioRender.com). (B) Behavioral performance of Sprague Dawley rats (n = 10) on a TOJ task plotted as proportion of “visual first” trials. Rats were exposed to either synchronous (A0V, black), 160 ms auditory-leading (A160V, red), or 160 ms visual-leading (V160A, dark red) stimuli prior to behavioral testing. (C) The point of subjective simultaneity (PSS) was extracted from the three fitted curves A160V, A0V, V160A. Consistent with humans, the PSS was shifted in the direction of the prior sensory experience. (D) The just noticeable difference (JND) of the three fitted curves did not change in response to the three passive exposure conditions. (E) Reaction time of rats for each SOA for the auditory-leading (A160V; red) and visual-leading (V160A; dark red) prior sensory experiences. Values are presented as mean ± SEM for PSS and JND, *p < 0.05, **p < 0.017.

Figure 2

Passive sensory exposure shifted perception while sparing audiovisual temporal acuity in rats performing the SJ task. (A) Schematic overview of the rat synchrony judgment (SJ) task within the operant chamber (created with BioRender.com). (B) Behavioral performance of Sprague Dawley rats (n = 12) on an SJ task plotted as proportion of “synchronous” trials. Rats were exposed to either synchronous (A0V, black), 210 ms auditory-leading (A210V, red), or 210 ms visual-leading (V210A, dark red) stimuli prior to behavioral testing. (C) The point of subjective simultaneity (PSS) was extracted from the three fitted curves A210V, A0V, V210A. Consistent with humans, the PSS was significantly shifted in the direction of the prior sensory experience. (D) The temporal binding window (TBW) of the three fitted curves did not change in response to the three passive exposure conditions. (E) Reaction time of rats for each SOA for the auditory-leading (A210V; red) and visual-leading (V210A; dark red) prior sensory experiences. Values are presented as mean ± SEM for PSS and TBW, *p < 0.05, **p < 0.017.

Figure 3

Rats showed evidence of rapid recalibration to asynchronous stimuli while performing the TOJ task. (A) Behavioral performance of Sprague Dawley rats (n = 11) on a temporal order judgment (TOJ) task plotted as proportion of “visual first” trials. Trials were separated into two categories, fitted then plotted: trials that followed an auditory-leading trial (light blue) or ones that followed a visual-leading trial (dark blue). (B) The point of subjective simultaneity (PSS) was extracted from the auditory-leading curve (A), visual-leading curve (V), and the combined curve which includes all trial types (C). As expected, the PSS was shifted in the direction of the previous trial. (C) The just noticeable difference (JND) of auditory-leading (A), combined trials (C), or visual-leading (V) curves did not change in response to the previous trial. (D) Reaction time of rats for each SOA for both auditory-leading (light blue) and visual-leading (dark blue) trials. (E) Relationship between the degree of change in PSS and the width of the JND, with the plotted line representing the liner regression fit. The change in PSS between visual-leading (V) and auditory-leading (A) trials were positively correlated with the width of the JND. Values are presented as mean ± SEM for PSS and TBW, *p < 0.05, **p < 0.0167 for (B) and (C), *p < 0.05. ** < 0.0071 for (D).

Figure 4

Rapid recalibration was not observed in rats performing the SJ task. (A) Behavioral performance of Sprague Dawley rats (n = 12) on a synchrony judgment (SJ) task plotted as proportion of “synchronous” trials. Trials were separated into two categories, fitted then plotted: trials that follow an auditory-leading trial (light blue) or ones that follow a visual-leading trial (dark blue). (B) The point of subjective simultaneity (PSS) was extracted from the auditory-leading curve (A), visual leading curve (V), and the combined curve which includes both trial types and synchronous trials (C). Unexpectedly, the rats performing the SJ task did not demonstrate rapid recalibration, as there was no shift in their PSS according to the preceding trial type. (C) The temporal binding window (TBW) of the three fitted curves, in which the TBW of auditory-leading (A) trials was significantly larger than the TBW of the combined curve (C), with no effect observed for visual-leading (V) TBW. (D) Reaction time of rats for each SOA for both auditory-leading (light blue) and visual-leading (dark blue) trials. Reaction time was not affected by the preceding trial. (E) For each rat, the degree of change in PSS was plotted against its TBW, with the line representing the liner regression fit. No correlation was observed for the change in PSS between visual-leading (V) and auditory-leading (A) trials and the TBW of the combined curve (C). Values are presented as mean ± SEM for PSS and TBW, *p < 0.05, **p < 0.017.

Figure 5

Background noise altered audiovisual temporal perception in rats performing the TOJ task. (A) Behavioral performance of Sprague Dawley rats (n = 10) on a temporal order judgment (TOJ) task plotted as proportion of “visual first” trials. Rats were either tested with a 60 dB SPL background noise played from a second speaker (Noise; green) or with no added background noise (Quiet; gray). (B) The point of subjective simultaneity (PSS) shifted to the left side of the psychometric curve in response to background noise. (C) The just noticeable difference (JND) of the fitted curves widened in response to background noise. (D) Reaction time of rats for each SOA for the background noise (green) or quiet control (gray) testing conditions. (E) The bounds of the JND values at the 25 and 75% proportions of “visual-first” responses. The left bound, but not the right, was significantly widened in response to background noise. Values are presented as mean ± SEM for PSS and TBW, *p < 0.05, **p < 0.0046.

Figure 6

Background noise did not significantly alter audiovisual temporal perception in rats performing the SJ task. (A) Behavioral performance of Sprague Dawley rats (n = 8) on a synchrony judgment (SJ) task plotted as proportion of “synchronous” trials. Rats were either tested with a 60 dB SPL background noise played from a second speaker (Noise; green) or with no added background noise (Quiet; gray). (B,C) The point of subjective simultaneity (PSS; panel B) and the temporal binding window (TBW; panel C) of the fitted curves did not shift in response to background noise. (D) Reaction time of rats for each SOA for the background noise (green) or quiet control (gray) testing conditions. (E) Assessment of the bounds of the TBW values at the 50% perceived synchronous trials from the center of the fitted curve revealed no change in response in the background noise versus quiet condition. Values are presented as mean ± SEM for PSS and TBW, *p < 0.05.

Figure 7

Disruption of glutamatergic neurotransmission impaired audiovisual temporal acuity in rats performing the TOJ task. (A) Behavioral performance of Sprague Dawley rats (n = 10) on a temporal order judgment (TOJ) task plotted as proportion of “visual first” trials. Rats were subcutaneously injected with MK-801 (0.1 mg/kg; orange) or a saline control (gray). (B) The point of subjective simultaneity (PSS) did not shift for the MK-801 treatment in comparison to the control treatment. (C) Compared to the control treatment, MK-801 caused an increase in the just noticeable difference (JND) of the fitted curves; evidence of a decrease in temporal acuity. (D) Reaction time of rats for each SOA for the MK-801 (orange) and control treatment (gray). (E) The bounds of the JND values at the 25 and 75% proportions of “visual-first” responses did not change between the two treatments. Values are presented as ± SEM for PSS and TBW, *p < 0.05.

Figure 8

Audiovisual temporal acuity, specifically during auditory-leading trials of the SJ task, was impaired following disruption of glutamatergic neurotransmission. (A) Behavioral performance of Sprague Dawley rats (n = 8) on an SJ task plotted as proportion of “synchronous” trials. Rats were subcutaneously injected with MK-801 (0.1 mg/kg; orange) or a saline control (gray). (B) The point of subjective simultaneity (PSS) shifted in the MK-801 treatment compared to the control treatment. (C) The temporal binding window (TBW) calculated from the fitted curves did not significantly differ between the two treatment conditions (p = 0.08). (D) Reaction time of rats for each SOA for the MK-801 (orange) and control treatment (gray). (E) MK-801 significantly changed the left bound of the TBW compared to the control treatment; suggesting that MK-801 exerted a greater effect on the rats’ ability to judge asynchronous stimuli when the auditory stimulus preceded the visual. Values are presented as mean ± SEM for PSS and TBW, *p < 0.05, **p < 0.017.