The cortical auditory system is far more extensive than expected, as it includes not only the entire superior temporal gyrus (STG) but also large portions of the parietal, prefrontal, and limbic lobes. Evidence from neuroimaging studies in monkeys from our lab and those of others have raised the possibility that, like occipitotemporal visual areas, superior temporal auditory areas send highly processed stimulus quality information to downstream targets via a multisynaptic corticocortical pathway that proceeds stepwise in a caudal-rostral direction. Yet, most of the evidence that has been gathered regarding serial auditory processing points to information flow orthogonal to the caudal-rostral axis. The medial geniculate nucleus sends projections to the auditory core areas (A1, R, and RT) on the supratemporal plane (STP), which then project to their laterally and medially adjacent neighbors in the auditory belt which, in turn, project laterally to the auditory parabelt. The evidence thus suggests that the core constitutes the first stage of cortical processing, with a serial progression from core outward, first to the belt and then to the parabelt. This progessing schema is also supported by neurophysiological evidence demonstrating that neurons in the anterolateral belt area (AL) are much more responsive to such sounds as band-passed noise, frequency-modulated sweeps, and monkey calls than they are to pure tones, suggesting that area AL is at a higher level of processing than medially adjacent core area R. Neuroanatomical data indicates that area AL is a source of direct projections to the ventrolateral prefrontal cortex suggesting that area AL is a late modality-specific cortical station. Comparatively little is known about the flow of information along the caudal-rostral dimension of STP. As previously described the STP is activated by sound, yet the inputs to the areas rostral to the core remain undefined. We hypothesized that the rostral STP receives input via stepwise serial projections from the core: from A1 through the rostral and rostrotemporal fields of the core (R and RT), continuing to the rostrotemporal (polar) field RTp. To test this proposal, we placed injections of neuroanatomical tracers into R, RT, and RTp. Injection of bi-directional tracers into area RTp reveals a feed-forward output to the TGd, and reciprocal connectivity with RT and R. Input to RTp arises from layers 2/3 and 5/6 of RT and R, as well as the belt fields flanking the core. In addition, fibers from RTp terminate in the rostral parabelt. Retrograde tracers injected in the rostral core reveal a primary feed-forward input from A1. These results support the proposal that caudal-rostral flow of auditory information from the core fields towards the temporal pole, and also reveal feedback connections within the STP and between the STP and parabelt. While our connectional data suggests a caudal-rostral processing along the STP little is known regarding the neuronal properties of the rostral STP, raising the question of what contribution this region makes to the processing of complex sounds. We have previously shown that this rostral region serves auditory discrimination and auditory short-term memory functions and appears to play a special role in processing conspecific calls. In a more recent study we compared the responses of rSTP and A1 neurons to a wide variety of sounds. We analyzed auditory responses of neurons in three different sectors distributed caudal-rostrally along the STP: Sector I, mainly area A1;Sector II, mainly area RT;and Sector III, principally RTp. Mean onset latency of excitation responses and stimulus selectivity to monkey calls and other sounds, both simple and complex, increased progressively from caudal-rostrally from Sector I to III. Also, whereas cells in Sector I responded with significantly higher firing rates to the other sounds than to monkey calls, those in Sectors II and III responded at the same rate to both stimulus types. The pattern of results support the proposal that the STP contains a rostrally directed, hierarchically organized auditory processing stream, with gradually increasing stimulus selectivity. We also recorded auditory evoked field potentials to macaque vocalizations from three chronically implanted micro-electrocorticographic arrays in the left hemisphere of one monkey. One array was positioned on an area estimated to be area A1, a second array was rostral on a part of area R and the third array was positioned on the parabelt lateral to A1. We observed auditory stimuli elicited spatiotemporally propagating waves of negative potentials across the STP and STG, with the dynamics of the waves depending on the acoustic properties of the stimulus. We next focused on the auditory evoked responses to 20 monkey vocalizations as well as control stimuli in which the spectrum carrier from each monkey vocalization was replaced by broadband noise (envelope-preserved vocalization). Our results suggest that complex spectral features of monkey vocalizations contribute to differential encoding particularly in higher auditory areas and differences in processing of species-specific vocalizations along caudal-to-rostral and medial-to-lateral axes. As part of our investigation of auditory processing we trained monkeys on a task designed to assess auditory recognition memory. The task is comparable to those used regularly to test visual recognition. The monkeys struggled to learn the auditory task taking on average more than 20,000 trials as compared with a few hundred trials typical of learning the task with visual stimuli. In addition performance on the auditory recognition task was unaffected by lesions of the rhinal cortex (Rh). These results have led us to the tentative conclusion that the monkeys were unimpaired after Rh lesions because they had performed the task utilizing working memory. We have since trained monkeys on different versions of the recognition memory task in attempts to improve performance and learn more about their auditory abilities. In each case it took the animals thousands of trials to learn and their forgetting threshold (75% performance level) remained less than 40 seconds. We did find that their auditory memory is stable over several seconds, but is highly susceptible to interference from even a single distracter stimulus. Errors are predicted by the spectral similarity of the sample and test stimulus, in the absence of an intervening """"""""distracter"""""""". The apparent failure in monkeys'auditory memory stands in contrast to the facility with which humans encode auditory stimuli in LTM, raising the question of whether the human ability is supported in some way by speech and language. Therefore we asked whether humans can store representations of sounds that can be neither repeated nor labeled. Subjects were presented with four lists of auditory stimuli differing in the degree to which speech or language could support encoding and storage in LTM: words, pseudowords, nonverbal sounds, and words played backwards. Recognition scores were highest for words (81%), somewhat lower for pseudowords and nonverbal sounds (each 75%), and lowest by far for reversed words (58%;with chance, 50%). Our results indicate that the more that articulation and verbal labeling can be used to support storage of auditory information in LTM, the better the performance appears to be. We have also begun assessing auditory memory in the KE family who have an inherited speech and language disorder. While basic auditory processes in the affected family members are normal, we suspect auditory LTM may be impaired because of the structural and functional abnormalities they have in Broca's and Wernicke's territories.
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