(1)The cortical auditory system is far more extensive than expected, as it includes not only the entire superior temporal gyrus but also large portions of the parietal, prefrontal, and limbic lobes. Several of these areas overlap with previously identified visual areas, suggesting that the auditory system, like the visual, contains separate pathways for processing stimulus quality and stimulus location as we have recently demonstrated with Human subjects when they were asked to remember the identity of voices or of their location in an fMRI study. (2) Anatomical evidence suggests that the auditory core constitutes the first stage of auditory cortical processing, with a serial progression from core outward, first to the surrounding auditory belt and then to the parabelt. The connectional evidence also suggests that the core itself (AI, R, and RT) is serially organized with a stepwise progression from A1 through R and RT to even more rostral parts of the supratemporal plane (STPr). We hypothesized that the STPr contains the anterior extension of a rostrally directed auditory pathway, and, in particular, that auditory subdivisions within the STPr form the continuation of a stimulus-quality processing stream originating in the auditory core area A1. In a recent electrophysiological study we analyzed single-unit activity, multi-unit activity, and local field potentials (LFP) distributed caudorostrally along the STP in: (i) caudal STP, including mainly A1; (ii) the middle part of STP (STPm); and (iii) the rostral part of STP (STPr), including cortex located within 3 mm of the tip of the temporal lobe. During recording sessions the animals performed an auditory task in which they discriminated between a positive stimulus (white noise) and any of 40 negative stimuli 20 monkey vocalizations and 20 other sounds which were the stimuli of interest. Our results demonstrated that the STP contains a rostrally directed, hierarchically organized auditory processing stream, with gradually increasing stimulus selectivity, and that this stream extends from the primary auditory area to the superior temporal pole. (3) To explore the effects of acoustic and behavioral context on neuronal responses in the core of auditory cortex (fields A1 and R), we trained monkeys on a go/no-go discrimination task in which they learned to respond selectively to a four-note target (S+) melody and withhold response to a variety of other nontarget (S-) sounds. We characterized two broad classes of neural activity that were modulated by task-performance. Class I consisted of tone-sequence-sensitive enhancement and suppression responses. Both facilitatory and suppressive responses in the trained monkeys showed a different temporal pattern from that observed in naive monkeys. Class II consisted of non-acoustic activity, characterized by a task-related component that correlated with the behavioral response leading to reward. We observed a significantly higher percentage of both Class I and Class II neurons in field R than in A1. Class I responses may help encode a long-term representation of the behaviorally salient target melody. Class II activity may reflect a variety of non-acoustic influences, such as attention, reward expectancy, somatosensory inputs, and/or motor set and may help link auditory perception and behavioral response. Both types of neuronal activity are likely to contribute to the performance of the auditory task. (3) Monkeys, like humans, appear to use the auditory system of the left hemisphere preferentially to process vocalizations. A voice region has recently been identified in the monkey auditory cortex with fMRI and electrophysiology, which shows a close functional correspondence to the known human-voice region. Both human and monkey voice regions lie anterior and superior on the temporal lobe and strongly prefer species-specific vocalizations over other categories of sounds and acoustical controls. The human and monkey voice regions are also sensitive to the vocal differences among individuals and appear to be important centers for vocal sound processing within a network that is poorly understood. We used microstimulation in combination with high-resolution fMRI to functionally localize the voice region, then we microstimulated the voice region and used the BOLD response to evaluate the anterograde targets of the microstimulation site. Microstimulation of the monkey voice region, which lies on the rostral superior-temporal plane (rSTP), elicited a BOLD response from hierarchically earlier auditory areas (feed-back), and the surrounding superior temporal plane (STP), gyrus (STG) and sulcus (STS) of the ipsilateral hemisphere. We observed no direct targets in the prefrontal cortex from voice region microstimulation, so we hypothesized that voice information might reach the frontal cortex indirectly. To test this idea we microstimulated a region in the upper bank of the STS that was one of the direct targets of the voice region, which resulted in medial and orbital prefrontal cortex activity, and neighboring regions on the STP, STG, STS and temporal pole. Our initial observations suggest that acoustical information from the voice region reaches the frontal cortex indirectly via other rostro-temporal regions such as the STS. (4) Monkeys trained on a task designed to assess auditory recognition memory, were impaired after removal of either the rostral superior temporal gyrus (rSTG) or the medial temporal lobe (MTL) but were unaffected by lesions of the rhinal cortex (Rh). These results compared with those obtained in other sensory modalities, in which Rh lesions produce severe impairment, lead to the tentative conclusion that the monkeys in this auditory study were unimpaired after Rh lesions because they had performed the task utilizing working memory. A normal monkey performing our version of auditory DMS resembles a monkey with Rh cortical lesions performing visual DMS; neither seems able to store long-term stimulus representations. This inability suggests that the auditory stimuli were processed without the participation of the Rh cortices and consequently ablating the Rh cortices had no deleterious effect. The correlate of this proposal is that, like the residual mnemonic ability in vision after Rh lesions, the mnemonic ability in audition observed here in normal monkeys rests entirely on mechanisms mediating short-term or working memory. This proposal that performance on our auditory DMS task was based on working memory implies it is the form of memory that impaired after both the rSTG and MT lesions. This implication after rSTG lesions is consistent with the anatomical position occupied by rSTG in the cortical auditory system. A series of anatomical studies suggests that rSTG may be a late station in the ventral processing stream for audition much like area TE is for vision, and so it is highly likely that rSTG serves an important role in short-term auditory memory just as area TE does in short-term visual memory. The impairment produced by the MT ablation may have been a result from collateral damage and not hippocampal damage, such as severing the projections of rSTG to downstream areas in the prefrontal cortex, medial thalamus, or both. We are now evaluating long-term auditory memory in chimpanzees to determine if this lack of auditory memory is specific to monkeys or extends to higher primates as well.
| Munoz, Monica; Mishkin, Mortimer; Saunders, Richard C (2009) Resection of the medial temporal lobe disconnects the rostral superior temporal gyrus from some of its projection targets in the frontal lobe and thalamus. Cereb Cortex 19:2114-30 |
| Poremba, Amy; Mishkin, Mortimer (2007) Exploring the extent and function of higher-order auditory cortex in rhesus monkeys. Hear Res 229:14-23 |
| Fritz, Jonathan; Mishkin, Mortimer; Saunders, Richard C (2005) In search of an auditory engram. Proc Natl Acad Sci U S A 102:9359-64 |
| Poremba, Amy; Saunders, Richard C; Crane, Alison M et al. (2003) Functional mapping of the primate auditory system. Science 299:568-72 |
| Elman, I; Sokoloff, L; Adler, C M et al. (1999) The effects of pharmacological doses of 2-deoxyglucose on cerebral blood flow in healthy volunteers. Brain Res 815:243-9 |
