Three psychophysical metrics of auditory temporal integration in macaques

Abstract

The relationship between sound duration and detection threshold has long been thought to reflect temporal integration. Reports of species differences in this relationship are equivocal: some meta-analyses report no species differences, whereas others report substantial differences, particularly between humans and their close phylogenetic relatives, macaques. This renders translational work in macaques problematic. To reevaluate this difference, tone detection performance was measured in macaques using a go/no-go reaction time (RT) task at various tone durations and in the presence of broadband noise (BBN). Detection thresholds, RTs, and the dynamic range (DR) of the psychometric function decreased as the tone duration increased. The threshold by duration trends suggest macaques integrate at a similar rate to humans. The RT trends also resemble human data and are the first reported in animals. Whereas the BBN did not affect how the threshold or RT changed with the duration, it substantially reduced the DR at short durations. A probabilistic Poisson model replicated the effects of duration on threshold and DR and required integration from multiple simulated auditory nerve fibers to explain the performance at shorter durations. These data suggest that, contrary to previous studies, macaques are uniquely well-suited to model human temporal integration and form the baseline for future neurophysiological studies.

Psychometric and subcortical neurometric measures of temporal discrimination in rhesus macaques

“…The effects of duration in this study extend work on auditory temporal integration to an AM discrimination paradigm, as opposed to more common tone detection paradigms (Costalupes, 1983; Heil et al, 2017; Mackey et al, 2021a; O’Connor et al, 1999; Plomp and Bouman, 1959). Temporal integration of AM stimuli has been explored almost exclusively at the psychophysical level, and mostly in humans (Dau et al, 1997; Lee, 1994; O’Connor et al, 2011; Sheft and Yost, 1990), though one study has reported causal evidence that parietal cortex is involved (Yao et al, 2020).…”

“…However, psychophysical studies have gained insight into auditory temporal integration by manipulating duration in AM processing tasks (Dau et al, 1997; Lee, 1994; O’Connor et al, 2011; Sheft and Yost, 1990). This question is of particular importance in the context of macaque studies, as macaques and budgerigars may exhibit unique similarity to humans in temporal integration (Mackey et al, 2021a). This motivated us to evaluate the effects of duration on performance in the AM frequency discrimination task previously discussed and explore its neural correlates.…”

“…Similarly, neurometric discrimination thresholds changed as the time-window used for spike-count analysis was changed (see Methods). The change in threshold as a function of duration is often quantified by the time constant (τ) of a three term exponential function (Mackey et al, 2021a; O’Connor et al, 1999), and is inversely related to the rate of integration. Thus, Figure 9 shows that CN neurons had, on average, slightly longer time constants than IC neurons, and neuronal time constants were longer than behavior.…”

“…Yao et al (2020) used a gerbil model, which permits the use of powerful genetic techniques. However, our previous work found that macaques and budgerigars exhibit unique similarity to humans in auditory temporal integration (Mackey et al, 2021a), which highlights the value of exploring these questions in a variety of animal models. The behavioral time constant reported here (30 ms) is almost identical to our previous report (Mackey et al, 2021a), and is much lower than the IC and CN (Figure 9), which suggests IC and CN integrate AM more slowly than macaques.…”

“…Current knowledge of subcortical AM processing draws heavily from rodent, cat, and budgerigar studies; however, a potential concern is the lack of subcortical AM processing studies in primates. Nonhuman primates bear exceptional similarity to humans in CN and cortical neuroanatomical structure (Hackett, 2011;Moore, 1980Moore, , 2000Moore et al, 1996; but see Rubio et al, 2008), perceptual measures of temporal processing (Kelly et al, 2006;Mackey et al, 2021a;Moody, 1994), auditory nerve frequency tuning (Joris et al, 2011;Verschooten et al, 2018), and cortical AM encoding (Hoglen et al, 2018). It is unclear to what degree the enhanced (relative to rodents) AM encoding in auditory cortex (Hoglen et al, 2018) is inherited from subcortical stations, because studies of subcortical AM processing in primates have been conducted under anesthesia (e.g.…”