An expanded role for the dorsal auditory pathway in sensorimotor control and integration

Abstract

The dual-pathway model of auditory cortical processing assumes that two largely segregated processing streams originating in the lateral belt subserve the two main functions of hearing: identification of auditory "objects", including speech; and localization of sounds in space (Rauschecker and Tian, 2000). Evidence has accumulated, chiefly from work in humans and nonhuman primates, that an antero-ventral pathway supports the former function, whereas a postero-dorsal stream supports the latter, i.e processing of space and motion-in-space. In addition, the postero-dorsal stream has also been postulated to subserve some functions of speech and language in humans. A recent review (Rauschecker and Scott, 2009) has proposed the possibility that both functions of the postero-dorsal pathway can be subsumed under the same structural forward model: an efference copy sent from prefrontal and premotor cortex provides the basis for "optimal state estimation" in the inferior parietal lobe and in sensory areas of the posterior auditory cortex. The current article corroborates this model by adding and discussing recent evidence.

Figure 1. Brain areas active during anticipatory imagery of familiar music

Activated brain regions are found in frontal and premotor regions, including inferior and superior frontal gyrus (IFG, SFG), pre-supplementary motor area (pre-SMA), as well as dorsal and ventral premotor cortex (dPMC, vPMC) (Leaver et al., 2009). Stimuli consisted of the final seconds of familiar or unfamiliar tracks from a compact disk (CD), followed by 8 s of silence. During the silence following familiar tracks from their favorite CD (anticipatory silence, AS, following familiar music, FM), subjects (Ss) reported experiencing anticipatory imagery for each subsequent track. Stimuli presented during unfamiliar trials consisted of music that the Ss had never heard before (unfamiliar music, UM). Thus, during this condition, Ss could not anticipate the onset of the following track (non-anticipatory silence, NS). While in the MRI scanner, subjects were instructed to attend to the stimulus being presented and to imagine, but not vocalize, the subsequent melody where appropriate.

Figure 2. Results of magnetoencephalography (MEG) measuring the effects of lip-reading and covert speech production on human auditory cortex responses

(Kauramäki et al., 2010). Auditory stimuli consisted of 50-ms tones of various frequencies presented in random order. While listening to the tones the subjects (Ss) performed one of four tasks: (1) “lip-reading”, i.e. Ss watched video clips of a face silently articulating Finnish vowels, (2) a visual control task of comparable difficulty (“expanding rings”), (3) a “still-face” passive control condition, and (4) “covert production” of the same vowels. During the still-face and covert-speech conditions, the Ss saw the same static face on the screen. During the expanding-rings as well as lip-reading conditions, Ss performed a one-back task. Auditory-cortex responses with a latency around 100 ms (N100m) were equally suppressed in the lip-reading and covert speech-production tasks compared with the visual control and baseline tasks; the effects involved all frequencies and were most prominent in the left hemisphere. Responses showed significantly increased N100m suppression immediately after the articulatory gesture. These findings suggest that the lip-reading-related suppression in the auditory cortex is caused by an efference copy from the speech-production system, generated during both own speech and lip-reading. The lower panel shows the mean (± standard error) differences in active task conditions relative to the passive still-face baseline. Asterisks indicate significant differences at a given frequency between the lip-reading vs. expanding-rings tasks (* p < 0.05, ** p < 0.01, *** p < 0.001).

Figure 3. Expanded model of dual auditory processing streams in the primate brain: a) Rhesus monkey (modified from Rauschecker and Tian, 2000); b) Human (simplified from Rauschecker and Scott, 2009)

While the role of the antero-ventral stream (green) in auditory object recognition, including perception of vocalizations and speech, is now widely accepted, the exact role of the postero-dorsal (or just “dorsal”) stream (red) is still being debated. Its function clearly includes spatial processing, but a role in human speech and language has also long been postulated. A reinterpretation of these classical studies suggests that the dorsal stream pivots around inferior/posterior parietal cortex, where a quick sketch of sensory event information is compared with an efference copy of motor plans (dashed lines). Thus, the dorsal stream plays a more general role in sensorimotor integration and control. In clockwise fashion, starting out from auditory cortex, the processing loop performs as a forward model: Object information, such as vocalizations and speech, is decoded in the antero-ventral stream all the way to category-invariant inferior frontal cortex (IFC, or VLPFC in monkeys) and transformed into articulatory representations (DLPFC or ventral PMC). Frontal activations are transmitted to the IPL and pST, where they are compared with auditory and other sensory information. It is this fronto-parietal-sensory section that turns the dorsal stream on its head and expands its fundtion. AC: auditory cortex; STS: superior temporal sulcus; IFC: inferior frontal cortex; PFC: prefrontal cortex; PMC: premotor cortex; IPL: inferior parietal lobule; IPS: inferior parietal sulcus; CS: central sulcus.