Ability of primary auditory cortical neurons to detect amplitude modulation with rate and temporal codes: neurometric analysis

Abstract

Amplitude modulation (AM) is a common feature of natural sounds, and its detection is biologically important. Even though most sounds are not fully modulated, the majority of physiological studies have focused on fully modulated (100% modulation depth) sounds. We presented AM noise at a range of modulation depths to awake macaque monkeys while recording from neurons in primary auditory cortex (A1). The ability of neurons to detect partial AM with rate and temporal codes was assessed with signal detection methods. On average, single-cell synchrony was as or more sensitive than spike count in modulation detection. Cells are less sensitive to modulation depth if tested away from their best modulation frequency, particularly for temporal measures. Mean neural modulation detection thresholds in A1 are not as sensitive as behavioral thresholds, but with phase locking the most sensitive neurons are more sensitive, suggesting that for temporal measures the lower-envelope principle cannot account for thresholds. Three methods of preanalysis pooling of spike trains (multiunit, similar to convergence from a cortical column; within cell, similar to convergence of cells with matched response properties; across cell, similar to indiscriminate convergence of cells) all result in an increase in neural sensitivity to modulation depth for both temporal and rate codes. For the across-cell method, pooling of a few dozen cells can result in detection thresholds that approximate those of the behaving animal. With synchrony measures, indiscriminate pooling results in sensitive detection of modulation frequencies between 20 and 60 Hz, suggesting that differences in AM response phase are minor in A1.

Encoding frequency contrast in primate auditory cortex

“…Most obviously, tuning for frequency and tuning for sound level are typically quite different at the level of individual cortical neurons (Brugge and Merzenich 1973;Recanzone et al 2000;Sadagopan andWang 2008, Scott et al 2011). Cortical FTFs are almost universally band pass for frequency and tend to be more sharply tuned than even the most highly nonmonotonic RLFs (e.g., Joris et al 2011). Differences in tuning to frequency and level predict distinct MPH shapes via simple lookup models (Malone et al Firing rate is assessed in terms of either the maximum firing rate obtained for a particular stimulus on the relevant function (e.g., the modulation depth function), or for the span of average firing rates (i.e., maximum vs. minimum) for the relevant function.…”

“…Further experiments will be required to determine how concurrent AM and FM are perceived (Ozimek and Sek 1987;Sek and Moore 1994) and represented by neural systems (Ding and Simon 2009). In particular, relating details of the cortical encoding model to perception will require further characterization of how information in cortical spike trains is integrated across neurons (Johnson et al 2012;Schneider and Woolley 2010), and over what time scales in different cortical regions (Scott et al 2011). Nevertheless, our data clearly demonstrate that moment-by-moment changes in frequency are robustly represented in moment-by-moment changes in the firing rates of cortical neurons, particularly at the modulation rates that dominate both macaque vocalizations and human speech (Cohen et al 2007;Elliott and Theunissen 2009;Rosen 1992), suggesting that cortical frequency coding is both dynamic and adaptive.…”

Midbrain Synchrony to Envelope Structure Supports Behavioral Sensitivity to Single-Formant Vowel-Like Sounds in Noise

“…Whereas the auditory nerve and nuclei of the brainstem encode amplitude-modulated (AM) sounds primarily through response synchrony to envelope structure (Joris and Yin 1992;Rhode and Greenberg 1994;Gleich and Klump 1995;Sayles et al 2013), neurons at the level of the IC or higher encode AM through both envelope synchrony and substantial changes in average rate as a function of the modulation properties of the stimulus (IC: Langner and Schreiner, 1988;Woolley and Casseday, 2005;thalamus: Bartlett and Wang, 2007;cortex: Rosen et al 2010;Yin et al 2011;Johnson et al 2012;reviewed in Joris et al 2004). In commonly occurring IC neurons with band-enhanced modulation tuning, average rate increases with modulation depth for AM sounds presented within a limited band of modulation frequencies (Krishna and Semple 2000; Nelson and Carney 2007).…”

Modulation-Frequency-Specific Adaptation in Awake Auditory Cortex

“…Numerous physiological studies have begun to clarify the cortical representations of modulated signals (for review, see Joris et al, 2004;, including substantial work in primate models (Bieser and Müller-Preuss, 1996;Lu et al, 2001;Liang et al, 2002;Bartlett and Wang, 2005;Malone et al, 2007Malone et al, , 2013Malone et al, , 2014Johnson et al, 2012). Here, we searched for cortical evidence of modulation masking in a forward-masking paradigm with SAM applied to tonal carriers in awake squirrel monkeys.…”