Romanski et al. (1999) - Nature Neuroscience

Romanski, L. M., Tian, B., Fritz, J., Mishkin, M., Goldman-Rakic, P. S., & Rauschecker, J. P. (1999). Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nature Neuroscience, 2(12), 1131–1136. https://doi.org/10.1038/16056

  • separate auditory streams originate in caudal and rostral auditory cortex and target spatial and non-spatial domains of the frontal lobe
  • three cochleotopically organized fields separated by frequency reversals, termed anterolateral (AL), middle-lateral (ML) and caudolateral (CL) areas, are mapped within the lateral belt17. Electrophysiological studies of the superior temporal region in nonhuman primates suggests that its anterior and posterior aspects may differ functionally
  • These findings raise the possibility that separate thalamocortical and corticocortical streams exist in the auditory system just as they do in the visual system
  • We recorded from the lateral auditory belt and parabelt cortices in the superior temporal region of four rhesus macaques and determined the best center frequency along each electrode penetration through lateral belt areas AL, ML and CL
  • The most anterior field, AL, had neuronal responses that ranged from 12.5 kHz at its most anterior edge down to 0.5 kHz where a frequency reversal occurred at its caudal edge, the point where area ML began. The best center frequencies in ML ranged from 0.5 kHz at its rostral edge to 20 kHz caudally just before the frequency reversal that marked the beginning of the caudal field, CL. The best frequencies in CL ranged from 20 kHz to 1 kHz. At the conclusion of the electrophysiological recordings, four to six distinguishable anatomical tracers were distributed among AL, ML and CL.
  • projections from area CL targeted the dorsal periarcuate cortex (area 8a, frontal eye fields) and the caudal principal sulcus (area 46) as well as the caudal inferior convexity (areas 12 vl and 45; Fig. 3b, c and e) and, in two cases, premotor cortex (area 6d). The frontal pole (area 10) and the lateral orbital cortices (areas 11 and 12) were devoid of anterograde labeling from injections into the caudal auditory region
  • frontal eye fields did not receive projections from anterior auditory area AL
  • AL and CL projections converged, revealed a rostrocaudal topography within these convergence zones such that rostral labeling in the principal sulcus and inferior convexity resulted from AL injections (Fig. 3a, b and e), whereas projections from area CL accounted for caudal labeling in these areas (Fig. 3b, c and e). ML projections were usually a combination of those from anterior and posterior fields and involved less of the extreme frontal pole and frontal eye fields but did label the principal sulcus, lateral inferior convexity and lateral orbital cortex (Fig. 3). These highly specific rostrocaudal topographical frontal–temporal connections suggest separate streams of auditory information that target distinct domains of the frontal lobes.
  • Projections from areas AL and ML were densest within the rostral parabelt and rostral temporal lobe, including the rostral supratemporal plane. In contrast, the posterior parietal cortex areas 7a and 7ip were labeled from injections only in CL. In addition, the medial belt regions and the caudal half of the dorsal bank of the superior temporal sulcus received dense projections from areas ML and CL but only light projections from AL.

discussion

  • One pathway, originating in CL, targets caudal dorsolateral prefrontal cortex (DLPFC); the other pathway, originating in AL, targets rostral and ventral prefrontal areas.
    • Because these dorsal and ventral prefrontal regions are respectively characterized as spatial and non-spatial functional domains2,27–29, a possible interpretation is that these separate streams originating from posterior and anterior auditory belt and parabelt cortices are analogous to the ‘where’ and ‘what’ streams of the visual system.
  • DLPFC also receives auditory afferents from the caudal auditory belt region, suggesting its involvement in auditory processing as well.
  • neuroimaging studies demonstrate involvement of the DLPFC in sound localization in humans
  • Neurons in AL of anesthetized monkeys presented with acoustic stimuli (consisting of vocalizations and band-passed noise from a variety of different azimuth locations in free field) show better selectivity for particular monkey calls, whereas neurons in CL had significantly narrower spatial tuning.
    • support the notion of an auditory spatial stream originating in the caudal belt and parabelt region and targeting the DLPFC. The caudal belt and parabelt are also connected to the DLPFC via the posterior parietal cortex, which is itself involved in the localization of both visual and auditory signals
  • In addition to this dorsal (and potentially ‘spatial’) auditory pathway, we present evidence for a second auditory stream originating in the anterior belt and parabelt region and terminating in the rostral and ventral frontal lobe. Neuroimaging studies demonstrate involvement of the frontal pole (area 10) of the rostral frontal lobe in verb generation, auditory working memory and musical consonance
  • Our results substantiate findings of a connection between the ventral prefrontal cortex and anterior auditory cortical regions
  • Ventrolateral frontal lobe regions 12 and 45, which make up the inferior convexity in the nonhuman primate, are situated just anterior to area 6, the premotor cortex43; it is suggested, on the basis of anatomical location and connections, that they represent the macaque homolog of Broca’s area4

see also

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Created: 2025-11-12 22:19