Dynamic Amplitude Coding in the Auditory Cortex of Awake Rhesus Macaques
Brian J. Malone, Brian H. Scott, Malcolm N. Semple
Journal of Neurophysiology
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 amplitude modulation (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 dB are robustly encoded by the cycle-by-cycle response dynamics evident in the MPH. We demonstrate that all of the parameters that define a SAM stimulus -carrier frequency, carrier level, modulation frequency, and modulation depthare 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 in order 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 below 20 Hz, the processing of modulated signals is better described as envelope shape discrimination rather than modulation frequency extraction. Page 5 of 86 in the range most important for communication sounds unequivocally encode changes in sound amplitude, and are robustly sensitive to all parameters defining the SAM signal. Materials and Methods: Subjects, surgical preparation, and physiological recording Two adult male monkeys (Macaca mulatta, designated X and Z) participated in these experiments. All procedures pertaining to animal use and welfare in this study were reviewed and approved by the New York University Institutional Animal Care and Use Committee. Prior to implant surgery, anesthesia was induced with ketamine and sodium thiopental, and a surgical plane was maintained with isoflurane. This first implant was a head-holder that mated to a specially designed primate chair (Crist Instruments, Hagerstown, MD). After behavioral training, a recording chamber (CalTech Engineering Services, Pasadena, CA) was implanted above the auditory cortex in the left hemisphere of each animal. The initial placement of the recording chamber on monkey Z was slightly rostral to allow recordings across the rostral (R) and rostrotemporal (RT) fields (Hackett, et al., 1998). The back of the initial chamber and the front of the chamber in its second placement straddled the low frequency portion of primary auditory cortex (AI). Upon completion of the mapping of the left hemisphere, the recording chamber was removed, and the skull was permitted to regrow under a protective layer of acrylic (Palacos). Meanwhile, a new recording chamber was implanted above the putative location of field R on the right hemisphere, which allowed for limited access to AI caudally. The initial implant for animal X was centered over AI in the left hemisphere, and allowed for a complete mapping of AI and portions of the surrounding auditory cortex. When this site was completed and covered, a new recording chamber was centered on the putative low-frequency border of AI/R in the right hemisphere. All penetrations were made vertically with respect to the cylinder implants, and thus roughly parallel to the stereotaxic vertical plane. Animal Z is still involved in experiments, so assignment of recording locations to cortical fields is based on physiological criteria, such as the tonotopic progression in AI, and the distribution of response latencies . Subsequent histology and post-mortem magnetic resonance imaging in animal X confirmed the recording locations to be within primary auditory cortex. We also assigned a relative cortical depth to the neurons in our sample by normalizing the recording depth with respect the first and last points in each penetration where audible "hash" responses could be detected (n = 270). Expressed in quintiles from the shallowest to deepest depths, we obtained the following distribution: 19%, 24%, 27%, 20%, and 10%. Although we cannot unequivocally assign our recordings to particular laminae, it is likely that the neurons in our sample came predominantly from the middle and upper layers. Both animals were extensively trained on binaural lateralization tasks. During recordings, blocks of psychophysical trials alternated with passive listening, when the SAM stimuli described in this report were presented. Behavioral and recording sessions were all conducted in a double-walled sound attenuated chamber (Industrial Acoustics Company) while the animals were continuously monitored via closed circuit television. Single unit activity was recorded with tungsten microelectrodes (FHC, Bowdoin, MA) advanced into the brain via a stepping motor microdrive (CalTech Engineering Services, Pasadena, CA). Recording location was referenced to a stereotaxic positioning system that mounted directly on the implant. Depths of all recordings were referenced to entry into the brain. Entry into the superior temporal plane was typically marked by a sudden increase in activity following a long silent interval, and the first appearance of auditory responsiveness.