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. The evidence suggests that the core (A1, R, and RT) constitutes the first stage of cortical processing, with a serial progression from core outward, first to the belt and then to the parabelt. Comparatively little is known about the flow of auditory information along the caudal-rostral dimension of the supratemporal plane (STP). More recent data suggests there is also a flow of information that follows a hierarchical processing scheme with the rostral auditory cortex receiving input via stepwise serial projections in the caudal to rostral dimension: through the primary (A1), rostral (R), and rostrotemporal core fields (RT) on the STP, continuing to the rostrotemporal polar field RTp. In addition to our investigation of the cortical connections we also investigated the subcortical connections of AI, R, RT, and RTp. Within the core, the balance of thalamocortical input shifts between A1 and R core fields: A1 receives a preponderance of thalamic input from the ventral division of the medial geniculate (MGv), R receives a mix of inputs from both the ventral and dorsal subdivisions (MGv and MGd, respectively), and inputs to RT skew more heavily towards MGd. RT and RTp also project to the MGd and MGv. Injections beyond the core fields in RTp, RPB, and STGr revealed thalamic inputs from outside the medial geniculate, including the suprageniculate nucleus and medial pulvinar. Additional projections were found to the striatum with RT and RTp projecting to the tail of the caudate nucleus and the adjacent ventral putamen. RTp also projects to the ventromedial region of the head of the caudate nucleus and nucleus accumbens. Finally, RT and RTp are strongly interconnected with the amygdala. In summary, auditory fields rostral to the core receive little input from the auditory thalamus, suggesting that their physiological responses to sound are mediated by the previously described corticocortical pathways. The subcortical connectivity establishes circuits by which auditory processing may interact with systems involved in learning, attention, reward, and emotion. One of the fundamental features of sensory cortex is that it topologically maps the physical attributes of sensory stimuli. In the macaque auditory cortex, the attribute mapped is sound frequency, yielding tonotopic maps in the core regions on the STP. While neural responses in these areas have been studied in detail, the spatiotemporal activation of these maps by acoustic stimuli has not. We designed a micro-electrocorticographic (ECoG) array to record field potentials simultaneously from multiple areas of macaque auditory cortex. We chronically implanted four such arrays on the surface of the STP as well as the caudal superior temporal gyrus. The arrays allowed us to record auditory evoked potentials from a large expanse of auditory cortex simultaneously with high temporal resolution, while the monkeys passively listened to 180 different pure tone stimuli. First we examined the auditory frequency tuning of auditory evoked potentials at conventional field potential frequency ranges. This analysis revealed tonotopic maps that reversed frequency direction at putative areal boundaries. Although all field potential frequency bands produced similar areal boundaries, the smoothest tonotopic-reversal map was obtained from the high-gamma band. Next, we estimated when each site showed significant discrimination among different stimulus frequencies by evaluating the high-gamma power in a 40 ms moving window. We found that the onset time of the discrimination increased along the caudal-to-rostral as well as the medial-to-lateral axes, consistent with the hypothesis that auditory information is serially processed in these two directions in parallel. 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. In contrast to learning a visual recognition the monkeys struggled to learn the auditory task. In addition performance on the auditory recognition task was unaffected by lesions of the rhinal cortex whereas performance on visual recognition is severely disrupted. These results have lead us to the tentative conclusion that the monkeys were unimpaired after rhinal lesions because they had performed the task utilizing working memory. In a follow-up experiment to further determine the capacity, specificity, and duration of the maintained representation of an auditory stimulus. Monkeys were trained on a serial delayed-match-to sample task analogous. Performance was accurate in the absence of distracters, but degraded severely after the presentation of intervening nonmatch stimuli. Manipulation of the inter-stimulus interval confirmed that the performance degradation was attributable to the appearance of the intervening stimuli, not the decay of memory over time. Analysis of performance by stimulus type showed a weak and counter-intuitive effect of sound category that favored simple stimuli (e.g., tones and noise) and not species-specific vocalizations. These results suggest a strong effect of retroactive interference, such that the nonmatch stimulus disrupted the maintained trace of the sample, effectively lowering the similarity criterion at which monkeys indicated a match. The present results suggest that the auditory working memory trace in nonhuman primates is fragile, and limited to one or two items. 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. 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. Half of the members of the multigenerational KE family have an inherited speech-language disorder, characterized mainly as a verbal and orofacial dyspraxia. The core phenotype of the affected KE members (aKE) is a deficit in repeating words, especially non-words, and in moving the orofacial musculature. It is not clear whether the speech deficit results from combined Working Memory (WM) and motor output problems, or from motor output difficulties alone. We assessed WM using a test battery based on the Baddeley and Hitch WM model. The model posits that the central executive (CE), important for planning and manipulating information, works in conjunction with two modality-specific components: The Phonological Loop (PL), and the Visuospatial Sketchpad (VSSP). We compared Results revealed only a significant Component x Group interaction. Our preliminary results indicate that the aKE, who have both structural and functional abnormalities in Brocas area, a structure known to be involved in phonological WM, may be specifically impaired in phonological WM, but not in CE or VSSP. This suggests that the word and non-word repetition difficulties of the aKE members may be influencing their motor-related representations required for internal rehearsal of speech-based material in phonological WM. While basic auditory processes in the affected family are normal we suspect auditory WM may be impaired because of the structural and functional abnormalities they have in Broca's and Wernicke's areas.

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20
Fiscal Year
2011
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$1,529,164
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U.S. National Institute of Mental Health
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Scott, Brian H; Mishkin, Mortimer (2016) Auditory short-term memory in the primate auditory cortex. Brain Res 1640:264-77
Karabanov, Anke Ninija; Paine, Rainer; Chao, Chi Chao et al. (2015) Participation of the classical speech areas in auditory long-term memory. PLoS One 10:e0119472
Petkov, Christopher I; Kikuchi, Yukiko; Milne, Alice E et al. (2015) Erratum: Different forms of effective connectivity in primate frontotemporal pathways. Nat Commun 6:7190
Petkov, Christopher I; Kikuchi, Yukiko; Milne, Alice E et al. (2015) Different forms of effective connectivity in primate frontotemporal pathways. Nat Commun 6:6000
Muñoz-López, M; Insausti, R; Mohedano-Moriano, A et al. (2015) Anatomical pathways for auditory memory II: information from rostral superior temporal gyrus to dorsolateral temporal pole and medial temporal cortex. Front Neurosci 9:158
Fritz, Jonathan B; Malloy, Megan; Mishkin, Mortimer et al. (2015) Monkey?s short-term auditory memory nearly abolished by combined removal of the rostral superior temporal gyrus and rhinal cortices. Brain Res :
Fukushima, Makoto; Saunders, Richard C; Fujii, Naotaka et al. (2014) Modeling vocalization with ECoG cortical activity recorded during vocal production in the macaque monkey. Conf Proc IEEE Eng Med Biol Soc 2014:6794-7
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Scott, Brian H; Mishkin, Mortimer; Yin, Pingbo (2014) Neural correlates of auditory short-term memory in rostral superior temporal cortex. Curr Biol 24:2767-75

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