Speech and language are considered uniquely human abilities: animals have communication systems, but they do not match human linguistic skills in terms of recursive structure and combinatorial power. Yet, in evolution, spoken language must have emerged from neural mechanisms at least partially available in animals. In this paper, we will demonstrate how our understanding of speech perception, one important facet of language, has profited from findings and theory in nonhuman primate studies. Chief among these are physiological and anatomical studies showing that primate auditory cortex, across species, shows patterns of hierarchical structure, topographic mapping and streams of functional processing. We will identify roles for different cortical areas in the perceptual processing of speech and review functional imaging work in humans that bears on our understanding of how the brain decodes and monitors speech. A new model connects structures in the temporal, frontal and parietal lobes linking speech perception and production.Our understanding of speech processing has both benefited and suffered from developments in neuroscience. The basic brain areas important for speech perception and production were established in the nineteenth century, and although our conception of their exact anatomy and function has changed substantially, some of the findings of Broca 1 and Wernicke 2 still stand (Supplementary Discussion 1 and Supplementary Fig. 1 online). What has lagged behind is a good model of how the brain decodes spoken language and how speech perception and speech production are linked. For example, the frameworks for cortical processes and pathways have taken longer to form in audition than in vision, and animal models of language have severe limitations 3 . The evolution of speech and language are likely to have depended on neural systems available in other primate brains. In this paper, we will demonstrate how our understanding of speech perception, one important facet of language, has profited from work in nonhuman primate studies. Streams and hierarchies in nonhuman primate auditory cortex'What' and 'where' pathways in vision and audition A decade ago, it was suggested that auditory cortical processing pathways are organized dually, similar to those in the visual cortex ( Fig. 1 the primary sensory areas into posterior parietal cortex, another pathway into anterior temporal cortex. As in the visual system 6 , the posterior parietal pathway was hypothesized to subserve spatial processing in audition while the temporal pathway subserved the identification of complex patterns or objects. Per the directions of their projections in the auditory system, these pathways were referred to as the postero-dorsal and antero-ventral streams, respectively.Anatomical tract tracing studies in monkeys support separate anterior and posterior projection streams in auditory cortex 7,8 . The long-range connections from the surrounding belt areas project from anterior belt directly to ventrolateral prefrontal cortex (PFC) an...

The functional specialization and hierarchical organization of multiple areas in rhesus monkey auditory cortex were examined with various types of complex sounds. Neurons in the lateral belt areas of the superior temporal gyrus were tuned to the best center frequency and bandwidth of band-passed noise bursts. They were also selective for the rate and direction of linear frequency modulated sweeps. Many neurons showed a preference for a limited number of species-specific vocalizations (''monkey calls''). These response selectivities can be explained by nonlinear spectral and temporal integration mechanisms. In a separate series of experiments, monkey calls were presented at different spatial locations, and the tuning of lateral belt neurons to monkey calls and spatial location was determined. Of the three belt areas the anterolateral area shows the highest degree of specificity for monkey calls, whereas neurons in the caudolateral area display the greatest spatial selectivity. We conclude that the cortical auditory system of primates is divided into at least two processing streams, a spatial stream that originates in the caudal part of the superior temporal gyrus and projects to the parietal cortex, and a pattern or object stream originating in the more anterior portions of the lateral belt. A similar division of labor can be seen in human auditory cortex by using functional neuroimaging.T he visual cortex of nonhuman primates is organized into multiple, functionally specialized areas (1, 2). Among them, two major pathways or ''streams'' can be recognized that are involved in the processing of object and spatial information (3). Originally postulated on the basis of behavioral lesion studies (4), these ''what'' and ''where'' pathways both originate in primary visual cortex V1 and are, respectively, ventrally and dorsally directed. Already in V1 neurons are organized in a domain-specific fashion, and separate pathways originate from these domains before feeding into the two major processing streams (5). Neurons in area V4, which is part of the ''what'' pathway or ventral stream, are highly selective for the color and size of visual objects (6, 7) and, in turn, project to inferotemporal areas containing complex visual object representations (8, 9). Neurons in area V5 (or MT), as part of the ''where'' pathway or dorsal stream, are highly selective for the direction of motion (10) and project to the parietal cortex, which is crucially involved in visual spatial processing (11-13). Both pathways eventually project to prefrontal cortex, where they end in separate target regions (14) but may finally converge (15). A similar organization has been reported recently for human visual cortex on the basis of neuroimaging studies (16,17).Compared with this elaborate scheme that has been worked out for visual cortical organization, virtually nothing has been known about the functional organization of higher auditory cortical pathways, even though a considerable amount of anatomical information had been collected early on (18 -2...

'What' and 'where' visual streams define ventrolateral object and dorsolateral spatial processing domains in the prefrontal cortex of nonhuman primates. We looked for similar streams for auditory-prefrontal connections in rhesus macaques by combining microelectrode recording with anatomical tract-tracing. Injection of multiple tracers into physiologically mapped regions AL, ML and CL of the auditory belt cortex revealed that anterior belt cortex was reciprocally connected with the frontal pole (area 10), rostral principal sulcus (area 46) and ventral prefrontal regions (areas 12 and 45), whereas the caudal belt was mainly connected with the caudal principal sulcus (area 46) and frontal eye fields (area 8a). Thus separate auditory streams originate in caudal and rostral auditory cortex and target spatial and non-spatial domains of the frontal lobe, respectively.

Neurons in the superior temporal gyrus of anesthetized rhesus monkeys were exposed to complex acoustic stimuli. Bandpassed noise bursts with defined center frequencies evoked responses that were greatly enhanced over those evoked by pure tones. This finding led to the discovery of at least one new cochleotopic area in the lateral belt of the nonprimary auditory cortex. The best center frequencies of neurons varied along a rostrocaudal axis, and the best bandwidths of the noise bursts varied along a mediolateral axis. When digitized monkey calls were used as stimuli, many neurons showed a preference for some calls over others. Manipulation of the calls' frequency structure and playback of separate components revealed different types of spectral integration. The lateral areas of the monkey auditory cortex appear to be part of a hierarchical sequence in which neurons prefer increasingly complex stimuli and may form an important stage in the preprocessing of communication sounds.