(1) The full extent of auditory tissue in the monkey brain was identified by comparing rates of glucose utilization in a 'hearing' hemisphere and a 'deafened' hemisphere of the awake animal while it listened passively to a wide variety of auditory stimuli. The cortical auditory system turned out to be far more extensive than expected, as it included not only the entire superior temporal gyrus but also large portions of the parietal, prefrontal, and limbic lobes. Several of these areas overlapped with previously identified visual areas, suggesting that the auditory system, like the visual, contains separate pathways for processing stimulus quality and stimulus location. (2) To test whether the neural substrates for auditory working memory, like those for visual working memory, would reflect this putative division of labor between stimulus quality and stimulus location processsing, we asked human subjects to remember the identity of voices or of their location in an fMRI study. The results supported the hypothesis in that, during the delay periods, activation was greater for voice location than for voice identity in dorsal prefrontal cortex, whereas the reverse was the case in ventral prefrontal cortex, a dissociatiion similar to the one found in vision during memory for faces vs. locations. (3) Little is known about the pattern of brain activity during processing of possible human language precursors, i.e., monkey vocalizations consisting of species-specific calls. Monkeys, like humans, appear to use the auditory system of the left hemisphere preferentially to process vocalizations. The neural basis of this functional asymmetry was investigated in monkeys by comparing metabolic rates, using [18F]2-fluro-2-deoxygucose and PET scanning, in the two hemispheres while the animals listened to conspecific calls compared with numerous other sound classes. Within the superior temporal gyrus, greater metabolic activity occurred on the left side than on the right only in the region of the temporal pole and only in response to monkey calls. This functional asymmetry was absent when the hemispheres were separated by forebrain commissurotomy, suggesting that the perception of vocalizations elicits concurrent interhemispheric interactions that focus the auditory processing within a specialized area of one hemisphere. (4) Monkeys trained preoperatively 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). Comparison of both the preoperative and postoperative results with those obtained in other sensory modalities, in which rhinal lesions produce severe impairment, lead to the tentative conclusion that the monkeys in this auditory study were unimpaired after rhinal lesions because they had performed the task utilizing short-term or working memory rather than long-term recognition memory. These results raise the question of whether they were the product of the particular procedures used here or whether instead the monkey's cerebral memory mechanisms in audition are intrinsically different from those in other sensory modalities. The comparisons of preoperative and postoperative performance indicate that a normal monkey performing our version of auditory DMS resembles a monkey with rhinal cortical lesions performing visual DMS, in the sense that neither seems able to store long-term stimulus representations. In the case of the normal monkey performing auditory DMS, this inability suggests that the auditory stimuli were processed without the participation of the rhinal cortices (or any other cortical tissue serving long-term memory in audition), and consequently ablating the rhinal cortices had no deleterious effect. The correlate of this proposal is that, like the residual mnemonic ability in vision after rhhinal 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 short-term or working memory implies that this is the form of memory that was impaired after both the rSTG and MT lesions. This suggestion is supported by the finding that the impairments were independent of delay interval, appearing at even the shortest interval tested. Moreover, the implication that the deficit after rSTG lesions was in short-term memory is consistent with the anatomical position occupied by rSTG in the cortical auditory system. That is, from a series of anatomical studies it appears 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. However, the implication that the impairment in Group MT likewise was in auditory short-term memory seems to contradict the well established view that the medial temporal lobe generally, and the hippocampal system in particular (i.e. hippocampus plus perirhinal, entorhinal, and parahippocampal cortices) is essential for long-term, not short-term, stimulus memory. In one case we had performed a complete removal of the hippocampal system, yet the auditory memory was preserved suggesting a possible resolution of the contradiction, namely, that the impairment produced by the MT ablation resulted not from damage to the hippocampal system but from collateral damage, such as severing the projections of rSTG to downstream areas in the prefrontal cortex, medial thalamus, or both. An anatomical study undertaken to examine this possibility demonstrated that an MT removal does indeed disconnect rSTG anatomically from several prefrontal and medial thalamic areas. (5) An important aspect of auditory processing is the spectral and temporal integration of acoustic information. To examine spectrotemporal integration in the primary auditory cortex of an awake rhesus monkey, we recorded neuronal responses to (a) pure tones and bandpassed noise in order to obtain frequency tuning curves (FTCs), (b) ripple stimuli in order to generate spectrotemporal receptive fields (STRFs), and (c) linear frequency modulated (FM) stimuli, which are natural components of monkey calls. In addition to the typical phasic onset responses observed in the anesthetized animal, primary cortical neurons in the awake monkey showed a variety of temporally structured types of response, including tonic, pauser, and offset responses, which appear to have different distributions in the two primary auditory areas, A1 and R. We also found evidence for greater spectral integration in primary auditory cortex than has previously been described in the anesthetized monkey. Although most of the neurons in the primary auditory cortex respond preferentially to a single best frequency, some neurons (10-15%) show multiple tuning peaks both in their FTCs and STRFs, suggesting that these neurons integrate spectral information over a wide range of frequencies, which is likely to be important in mediating auditory pattern recognition. Also, 75% of A1 and R neurons were selective for FM direction and/or rate, with response distributions suggesting that rate and directionality are independently represented in monkey primary auditory cortex.
| 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 |
