Frequency-Modulation Encoding in the Primary Auditory Cortex of the Awake Owl Monkey

Abstract

Many communication sounds, such as New World monkey twitter calls, contain frequency-modulated (FM) sweeps. To determine how this prominent vocalization element is represented in the auditory cortex we examined neural responses to logarithmic FM sweep stimuli in the primary auditory cortex (AI) of two awake owl monkeys. Using an implanted array of microelectrodes we quantitatively characterized neuronal responses to FM sweeps and to random tone-pip stimuli. Tone-pip responses were used to construct spectrotemporal receptive fields (STRFs). Classification of FM sweep responses revealed few neurons with high direction and speed selectivity. Most neurons responded to sweeps in both directions and over a broad range of sweep speeds. Characteristic frequency estimates from FM responses were highly correlated with estimates from STRFs, although spectral receptive field bandwidth was consistently underestimated by FM stimuli. Predictions of FM direction selectivity and best speed from STRFs were significantly correlated with observed FM responses, although some systematic discrepancies existed. Last, the population distributions of FM responses in the awake owl monkey were similar to, although of longer temporal duration than, those in the anesthetized squirrel monkeys.

Auditory frequency perception adapts rapidly to the immediate past

“…Previous adaptation studies have demonstrated that prolonged exposure to auditory stimuli with changing frequency increases the threshold for frequency modulation (Gardner & Wilson, 1979;Green & Kay, 1973;Kay & Matthews, 1972;Kayahara, 2001;Masutomi & Kashino, 2013;Regan & Tansley, 1979;Shu, Swindale, & Cynader, 1993;Tansley & Suffield, 1983), supporting the existence of neural populations tuned to frequency modulation. Confirming this psychophysical inference, neurophysiological studies have found neuronal populations tuned to frequency-modulation in a direction-selective manner in cats (Mendelson & Cynader, 1985;Mendelson & Grasse, 1992;Mendelson, Schreiner, Sutter, & Grasse, 1993), monkeys (Atencio et al, 2007;L. Liang, Lu, & Wang, 2002;Tian & Rauschecker, 2004), guinea pigs (Zhao & Liang, 1996), and bats (Gordon & O'Neill, 1998), and in humans using neuroimaging techniques (Pardo & Sams, 1993;Sams et al, 1991).…”

Detection of spatial cues in linear and logarithmic frequency-modulated sweeps

“…New World monkey vocalizations (e.g., twitter calls), for example, have been shown to contain FM transitions with rates between 30 and 50 octaves per second (Atencio et al, 2007;Bieser, 1998;Cheung, Bedenbaugh, Nagarajan, & Schreiner, 2001;Nagarajan et al, 2002;Wang, Merzinich, Beitel, & Schreiner, 1995). The role of frequency sweeps in animal communication has also been studied to determine its effect on object identification and informational unmasking (e.g., in nonhuman primates; Egnor, Iguina, & Hauser, 2006;Egnor, Wickelgren, & Hauser, 2007;Petkov, O'Connor, & Sutter, 2003).…”

Heterogeneous Neuronal Responses to Frequency-Modulated Tones in the Primary Auditory Cortex of Awake Cats

“…About four decades ago, Whitfield and Evans (1965) reported the presence of multiple FM response types in cat primary auditory cortex (A1) and qualitatively categorized them into four classes: 1) the cells commenced firing as a FM tone crossed the boundary into its TRF and continued to fire until it left; 2) the cells started and ceased firing when FM tones were wholly within TRF; 3) the cells fired when the FM tone was outside TRF; 4) the cells responded to FM tones, but not to steady tones. The recent study on the A1 of awake monkeys (Atencio et al 2007) also reported the presence of a sustained discharge mechanism responding to FM stimuli. Thus FM responses in awake A1 were more complicated than under anesthesia.…”

“…Suga and his colleagues (Edamatsu et al 1989;O'Neill and Suga 1982;Tsuzuki and Suga 1988) have conducted such experiments on awake bats and found that neuronal responses to particular aspects of FM stimuli, a crucial component of the bat's biosonar system, are topographically organized in the auditory cortex. To date, only two studies have been conducted on common mammals lacking acoustic specialization: a pioneering study on awake cats (Whitfield and Evans 1965) and a recent study on awake owl monkeys (Atencio et al 2007). About four decades ago, Whitfield and Evans (1965) reported the presence of multiple FM response types in cat primary auditory cortex (A1) and qualitatively categorized them into four classes: 1) the cells commenced firing as a FM tone crossed the boundary into its TRF and continued to fire until it left; 2) the cells started and ceased firing when FM tones were wholly within TRF; 3) the cells fired when the FM tone was outside TRF; 4) the cells responded to FM tones, but not to steady tones.…”