Transformation of Temporal Processing Across Auditory Cortex of Awake Macaques

Scott, Brian H.; Malone, Brian J.; Semple, Malcolm N.

doi:10.1152/jn.01120.2009

Cited by 73 publications

(123 citation statements)

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“…These units should also be selective for specific phoneme orderings. Nonhuman primate data for regions rostral to A1 confirm that latencies increase rostrally along the ventral stream (34,55,68,69), with the median latency to peak response approaching 100 ms in area RT (34), consistent with the latencies required for phonetic concatenation. In a rare human electrophysiology study, Creutzfeldt and colleagues (1989) report vigorous single-unit responses to words and sentences in mid-to anterior STG (70).…”

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confidence: 55%

Phoneme and word recognition in the auditory ventral stream

DeWitt

Rauschecker²

2012

Proc. Natl. Acad. Sci. U.S.A.

419

328

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Spoken word recognition requires complex, invariant representations. Using a meta-analytic approach incorporating more than 100 functional imaging experiments, we show that preference for complex sounds emerges in the human auditory ventral stream in a hierarchical fashion, consistent with nonhuman primate electrophysiology. Examining speech sounds, we show that activation associated with the processing of short-timescale patterns (i.e., phonemes) is consistently localized to left mid-superior temporal gyrus (STG), whereas activation associated with the integration of phonemes into temporally complex patterns (i.e., words) is consistently localized to left anterior STG. Further, we show left midto anterior STG is reliably implicated in the invariant representation of phonetic forms and that this area also responds preferentially to phonetic sounds, above artificial control sounds or environmental sounds. Together, this shows increasing encoding specificity and invariance along the auditory ventral stream for temporally complex speech sounds.functional MRI | meta-analysis | auditory cortex | object recognition | language S poken word recognition presents several challenges to the brain. Two key challenges are the assembly of complex auditory representations and the variability of natural speech (SI Appendix, Fig. S1) (1). Representation at the level of primary auditory cortex is precise: fine-grained in scale and local in spectrotemporal space (2, 3). The recognition of complex spectrotemporal forms, like words, in higher areas of auditory cortex requires the transformation of this granular representation into Gestalt-like, object-centered representations. In brief, local features must be bound together to form representations of complex spectrotemporal contours, which are themselves the constituents of auditory "objects" or complex sound patterns (4, 5). Next, representations must be generalized and abstracted. Coding in primary auditory cortex is sensitive even to minor physical transformations. Object-centered coding in higher areas, however, must be invariant (i.e., tolerant of natural stimulus variation) (6). For example, whereas the phonemic structure of a word is fixed, there is considerable variation in physical, spectrotemporal form-attributable to accent, pronunciation, body size, and the like-among utterances of a given word. It has been proposed for visual cortical processing that a feed-forward, hierarchical architecture (7) may be capable of simultaneously solving the problems of complexity and variability (8-12). Here, we examine these ideas in the context of auditory cortex.In a hierarchical pattern-recognition scheme (8), coding in the earliest cortical field would reflect the tuning and organization of primary auditory cortex (or core) (2, 3, 13). That is, single-neuron receptive fields (more precisely, frequency-response areas) would be tuned to particular center frequencies and would have minimal spectrotemporal complexity (i.e., a single excitatory zone and one-to-two inhibitory side bands). ...

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confidence: 55%

Phoneme and word recognition in the auditory ventral stream

DeWitt

Rauschecker²

2012

Proc. Natl. Acad. Sci. U.S.A.

419

328

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“…The paper leaves the reader wanting additional discussion of what greater latencies mean, and how temporal synchronization of firing rates may transform into a rate code as information passes between cortical areas in a processing stream. Scott et al (2011) show that AI and R are ostensibly very similar, having similar selectivity for tone frequency and intensity, similar baseline, threshold, and driven firing rates, and similar, yet reversed, tonotopic organization. The salient difference between AI and R, argue the authors, is temporal processing.…”

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confidence: 83%

“…How these divergent streams or substreams integrate spectrotemporal features of sound stimuli from lower brain areas into complete auditory perceptions remains a fundamental question in auditory neurophysiology. Scott et al (2011) argue for the hypothesis that temporal elements of a sound are processed caudorostrally inside the lateral fissure. This study focuses on core subfields AI and R, placing the two areas in the context of a hierarchical processing stream that extends along the STP and providing preliminary evidence for how these subfields might function within that stream.…”

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confidence: 99%

“…This begs the question, what roles do early auditory cortical areas play in representing or in developing auditory perception, and how do these roles differ among neuroanatomically defined areas of auditory cortex? This neuroforum article examines how Scott et al (2011) address this question by studying temporal processing among several early auditory cortical areas.Macaque auditory cortex is separated into three main regions ( Fig. 1): the core, belt, and parabelt.…”

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confidence: 99%

“…Does this mean there are two "ventral" processing streams, one on the STG and one on the STP, or are these two streams elements of a larger processing stream for stimulus quality or identity? Studies examining early stages of auditory cortical processing, such as Scott et al (2011) and Rauschecker et al (1997) in the macaque and Bendor and Wang (2008) in the marmoset, have led some researchers to hypothesize that temporal processing occurs hierarchically along the STP, whereas spectral elements of a sound are processed hierarchically from core to belt to parabelt . How these divergent streams or substreams integrate spectrotemporal features of sound stimuli from lower brain areas into complete auditory perceptions remains a fundamental question in auditory neurophysiology.…”

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Temporal processing in the auditory core: transformation or segregation?

Smith

2011

Journal of Neurophysiology

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Smith EH. Temporal processing in the auditory core: transformation or segregation?. J Neurophysiol 106: 2791-2793, 2011. First published July 27, 2011 doi:10.1152/jn.00233.2011.-Scott et al. (J Neurophysiol 105: 712-730, 2011) examine temporal processing in auditory Core fields AI and R in the macaque, arguing that temporal properties are the most salient functional differences between these areas. How these results imply transformation of information between AI and R or whether these fields may be processing divergent information somewhat separately is discussed. auditory cortex; processing stream; transformation of information THE CLASSIC VIEW OF PRIMARY auditory cortex is of a "whiteboard" (Nelken 2008), containing a complete, yet deconstructed, representation of an incoming soundwave. This information is then synthesized through the auditory cortical circuit to form auditory perception. It has since become clear that neural responses in early auditory cortex are more than the sum of their spectrotemporal parts, being influenced by stimulus or task context (Ghazanfar et al. 2005;Otazu et al. 2009). Since most deconstruction of acoustic information has been accomplished at the stage of the inferior colliculus (IC), the IC could be thought of as the auditory analog to primary visual cortex (Nelken 2008). This begs the question, what roles do early auditory cortical areas play in representing or in developing auditory perception, and how do these roles differ among neuroanatomically defined areas of auditory cortex? This neuroforum article examines how Scott et al. (2011) address this question by studying temporal processing among several early auditory cortical areas.Macaque auditory cortex is separated into three main regions ( Fig. 1): the core, belt, and parabelt. The core field contains three subfields, the primary auditory cortex (AI), the rostral field (R), and the rostrotemporal field (RT). These fields are arranged tonotopically, that is, by their selectivity to stimulus frequency. Reversals in tonotopic gradients have mainly been used to define borders between AI, R, and RT. The belt field contains eight subfields and the parabelt field consists of broadly defined rostral and caudal aspects (Hackett 2011). It has been hypothesized that auditory processing is organized into two streams, analogous to the dorsal and ventral processing streams in the visual system (Rauschecker and Scott 2009). That is, hierarchical auditory processing for sound location is directed caudally from the primary auditory cortex to the parietal lobe, and information about sound identity is directed rostrally along the superior temporal gyrus (STG). This hypothesis is supported by neuroanatomical studies showing that adjacent belt areas are more densely connected and mostly feed-forward (Hackett 2011). Anterior belt and parabelt then connect to anterior temporal lobe and ventrolateral prefrontal areas (Romanski et al. 1999).There is also neuroanatomical evidence for a hierarchical processing stream extending along the superior ...

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Thalamic connections of the core auditory cortex and rostral supratemporal plane in the macaque monkey

Scott

Saleem

Kikuchi

et al. 2017

J of Comparative Neurology

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In the primate auditory cortex, information flows serially in the mediolateral dimension from core, to belt, to parabelt. In the caudorostral dimension, stepwise serial projections convey information through the primary, rostral, and rostrotemporal (AI, R, and RT) core areas on the supratemporal plane, continuing to the rostrotemporal polar area (RTp) and adjacent auditory-related areas of the rostral superior temporal gyrus (STGr) and temporal pole. In addition to this cascade of corticocortical connections, the auditory cortex receives parallel thalamocortical projections from the medial geniculate nucleus (MGN). Previous studies have examined the projections from MGN to auditory cortex, but most have focused on the caudal core areas AI and R. In this study, we investigated the full extent of connections between MGN and AI, R, RT, RTp, and STGr using retrograde and anterograde anatomical tracers. Both AI and R received nearly 90% of their thalamic inputs from the ventral subdivision of the MGN (MGv; the primary/lemniscal auditory pathway). By contrast, RT received only ∼45% from MGv, and an equal share from the dorsal subdivision (MGd). Area RTp received ∼25% of its inputs from MGv, but received additional inputs from multisensory areas outside the MGN (30% in RTp vs. 1-5% in core areas). The MGN input to RTp distinguished this rostral extension of auditory cortex from the adjacent auditory-related cortex of the STGr, which received 80% of its thalamic input from multisensory nuclei (primarily medial pulvinar). Anterograde tracers identified complementary descending connections by which highly processed auditory information may modulate thalamocortical inputs.

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Transformation of Temporal Processing Across Auditory Cortex of Awake Macaques

Cited by 73 publications

References 72 publications

Phoneme and word recognition in the auditory ventral stream

Phoneme and word recognition in the auditory ventral stream

Temporal processing in the auditory core: transformation or segregation?

Thalamic connections of the core auditory cortex and rostral supratemporal plane in the macaque monkey

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