In many animals, the information most important for processing communication sounds, including speech, consists of temporal envelope cues below approximately 20 Hz. Physiological studies, however, have typically emphasized the upper limits of modulation encoding. Responses to sinusoidal AM (SAM) are generally summarized by modulation transfer functions (MTFs), which emphasize tuning to modulation frequency rather than the representation of the instantaneous stimulus amplitude. Unfortunately, MTFs fail to capture important but nonlinear aspects of amplitude coding in the central auditory system. We focus on an alternative data representation, the modulation period histogram (MPH), which depicts the spike train folded on the modulation period of the SAM stimulus. At low modulation frequencies, the fluctuations of stimulus amplitude in decibels are robustly encoded by the cycle-by-cycle response dynamics evident in the MPH. We show that all of the parameters that define a SAM stimulus--carrier frequency, carrier level, modulation frequency, and modulation depth--are reflected in the shape of cortical MPHs. In many neurons that are nonmonotonically tuned for sound amplitude, the representation of modulation frequency is typically sacrificed to preserve the mapping between the instantaneous discharge rate and the instantaneous stimulus amplitude, resulting in two response modes per modulation cycle. This behavior, as well as the relatively poor tuning of cortical MTFs, suggests that auditory cortical neurons are not well suited for operating as a "modulation filterbank." Instead, our results suggest that <20 Hz, the processing of modulated signals is better described as envelope shape discrimination rather than modulation frequency extraction.

The anatomy and connectivity of the primate auditory cortex has been modeled as a core region receiving direct thalamic input surrounded by a belt of secondary fields. The core contains multiple tonotopic fields (including the primary auditory cortex, AI, and the rostral field, R), but available data only partially address the degree to which those fields are functionally distinct. This report, based on single-unit recordings across four hemispheres in awake macaques, argues that the functional organization of auditory cortex is best understood in terms of temporal processing. Frequency tuning, response threshold, and strength of activation are similar between AI and R, validating their inclusion as a unified core, but the temporal properties of the fields clearly differ. Onset latencies to pure tones are longer in R (median, 33 ms) than in AI (20 ms); moreover, synchronization of spike discharges to dynamic modulations of stimulus amplitude and frequency, similar to those present in macaque and human vocalizations, suggest distinctly different windows of temporal integration in AI (20-30 ms) and R (100 ms). Incorporating data from the adjacent auditory belt reveals that the divergence of temporal properties within the core is in some cases greater than the temporal differences between core and belt.

A stimulus trace may be temporarily retained either actively [i.e., in working memory (WM)] or by the weaker mnemonic process we will call passive short-term memory, in which a given stimulus trace is highly susceptible to "overwriting" by a subsequent stimulus. It has been suggested that WM is the more robust process because it exploits long-term memory (i.e., a current stimulus activates a stored representation of that stimulus, which can then be actively maintained). Recent studies have suggested that monkeys may be unable to store acoustic signals in long-term memory, raising the possibility that they may therefore also lack auditory WM. To explore this possibility, we tested rhesus monkeys on a serial delayed match-to-sample (DMS) task using a small set of sounds presented with ∼1-s interstimulus delays. Performance was accurate whenever a match or a nonmatch stimulus followed the sample directly, but it fell precipitously if a single nonmatch stimulus intervened between sample and match. The steep drop in accuracy was found to be due not to passive decay of the sample's trace, but to retroactive interference from the intervening nonmatch stimulus. This "overwriting" effect was far greater than that observed previously in serial DMS with visual stimuli. The results, which accord with the notion that WM relies on long-term memory, indicate that monkeys perform serial DMS in audition remarkably poorly and that whatever success they had on this task depended largely, if not entirely, on the retention of stimulus traces in the passive form of shortterm memory.macaque | primate | vocalization W orking memory (WM) is a system that enables the temporary maintenance and manipulation of information necessary to guide behavior (1, 2). The term "working memory" has sometimes been applied to parametric sensory discriminations (3) [e.g., comparing the acoustic frequency of two successive tones, or the visual contrast of two successive images, separated by a short interstimulus interval (ISI)]. However, in the absence of the need for maintaining and manipulating the stimuli, such discriminations may be more properly described as tests of a type of shortterm memory (STM) that we will call passive short-term memory (pSTM) rather than WM.Definitions and models of WM vary (4), but the concepts of STM (particularly pSTM) and WM differ along a dimension of increasing attention to the stimulus item and greater reliance on its stored representation. Indeed, WM has been posited to differ from other forms of STM by operating not on a recently presented item, per se, but on the activation of a representation of that item stored in long-term memory (LTM) (4-7). This distinction is related to another, viz. the distinction between categorical perception and continuous, noncategorical perception, the former term implying that perception of some stimuli activates their previously stored representations sorted into categories on the basis of either their physical similarity or some more abstract factor. The capacity of WM in vision has b...

In the ascending auditory pathway, the context in which a particular stimulus occurs can influence the character of the responses that encode it. Here we demonstrate that the cortical representation of a binaural cue to sound source location is profoundly context-dependent: spike rates elicited by a 0 degrees interaural phase disparity (IPD) were very different when preceded by 90 degrees versus -90 degrees IPD. The changes in firing rate associated with equivalent stimuli occurring in different contexts are comparable to changes in discharge rate that establish cortical tuning to the cue itself. Single-unit responses to trapezoidally modulated IPD stimuli were recorded in the auditory cortices of awake rhesus monkeys. Each trapezoidal stimulus consisted of linear modulations of IPD between two steady-state IPDs differing by 90 degrees. The stimulus set was constructed so that identical IPDs and sweeps through identical IPD ranges recurred as elements of disparate sequences. We routinely observed orderly context-induced shifts in IPD tuning. These shifts reflected an underlying enhancement of the contrast in the discharge rate representation of different IPDs. This process is subserved by sensitivity to stimulus events in the recent past, involving multiple adaptive mechanisms operating on timescales ranging from tens of milliseconds to seconds. These findings suggest that the cortical processing of dynamic acoustic signals is dominated by an adaptive coding strategy that prioritizes the representation of stimulus changes over actual stimulus values. We show how cortical selectivity for motion direction in real space could emerge as a consequence of this general coding principle.

Currently there is considerable debate as to the nature of the pathways that are responsible for the perception and motor performance. We have studied the relationship between perceived speed, which is the experiential representation of a moving stimulus, and the speed of smooth pursuit eye movements, the motor action. We determined psychophysical thresholds for detecting small perturbations in the speed of moving patterns, and then by an ideal observer analysis computed analogous "oculometric" thresholds from the eye movement traces elicited by the same stimuli on the same trials. Our results confirm those of previous studies that show a remarkable agreement between perceptual judgments for speed discrimination and the fine gradations in eye movement speed. We analyzed the initial pursuit period of long duration (1000 ms) and short (200 ms) duration perturbations. When we compared the errors for perception and pursuit on a trial-by-trial basis there was no correlation between perceptual errors and eye movement errors. The observation that both oculometric and psychometric performance were similar, with Weber fractions in the normal range, but that there is no correlation in the errors suggests that the motor system and perception share the same constraints in their analysis of motion signals, but act independently and have different noise sources. We simulated noise in two models of perceptual and eye movement performance. In the first model we postulate an initial common source for the perceptual and eye movement signals. In that case about ten times the observed noise is required to produce no correlation in trial-by-trial performance. In the second model we postulate that the perceptual signal is a combination of a reafferent eye velocity signal plus the perturbation signal while the pursuit signal is derived from the oculomotor plant plus the perturbation signal. In this model about three times the noise level in the independent signals will mask any correlation due to the common perturbation signal.

Primary auditory cortex plays a crucial role in spatially directed behavior, but little is known about the effect of behavioral state on the neural representation of spatial cues. Macaques were trained to discriminate binaural cues to sound localization, eventually allowing measurement of thresholds comparable to human hearing. During behavior and passive listening, single units in low-frequency auditory cortex showed robust and consistent tuning to interaural phase difference (IPD). In most neurons, behavior exerted an effect on peak discharge rate (58% increased, 13% decreased), but this was not accompanied by a detectable shift in the best IPD of any cell. Neurometric analysis revealed a difference in discriminability between the behaving and passive condition in half of the sample (52%), but steepening of the neurometric function (29%) was only slightly more common than flattening (23%). This suggests that performance of a discrimination task does not necessarily confer an advantage in understanding the representation of the spatial cue in primary auditory cortex but nevertheless revealed some physiological effects. These results suggest that responses observed during passive listening provide a valid representation of neuronal response properties in core auditory cortex.

Summary Background Auditory short-term memory (STM) in the monkey is less robust than visual STM and may depend on a retained sensory trace, which is likely to reside in the higher-order cortical areas of the auditory ventral stream. Results We recorded from the rostral superior temporal cortex as monkeys performed serial auditory delayed-match-to-sample (DMS). A subset of neurons exhibited modulations of their firing rate during the delay between sounds, during the sensory response, or both. This distributed subpopulation carried a predominantly sensory signal modulated by the mnemonic context of the stimulus. Excitatory and suppressive effects on match responses were dissociable in their timing, and in their resistance to sounds intervening between the sample and match. Conclusions Like the monkeys’ behavioral performance, these neuronal effects differ from those reported in the same species during visual DMS, suggesting different neural mechanisms for retaining dynamic sounds and static images in STM.

In the ventral stream of the primate auditory cortex, cortico-cortical projections emanate from the primary auditory cortex (AI) along 2 principal axes: one mediolateral, the other caudorostral. Connections in the mediolateral direction from core, to belt, to parabelt, have been well described, but less is known about the flow of information along the supratemporal plane (STP) in the caudorostral dimension. Neuroanatomical tracers were injected throughout the caudorostral extent of the auditory core and rostral STP by direct visualization of the cortical surface. Auditory cortical areas were distinguished by SMI-32 immunostaining for neurofilament, in addition to established cytoarchitectonic criteria. The results describe a pathway comprising step-wise projections from AI through the rostral and rostrotemporal fields of the core (R and RT), continuing to the recently identified rostrotemporal polar field (RTp) and the dorsal temporal pole. Each area was strongly and reciprocally connected with the areas immediately caudal and rostral to it, though deviations from strictly serial connectivity were observed. In RTp, inputs converged from core, belt, parabelt, and the auditory thalamus, as well as higher order cortical regions. The results support a rostrally directed flow of auditory information with complex and recurrent connections, similar to the ventral stream of macaque visual cortex.