Neural latencies across auditory cortex of macaque support a dorsal stream supramodal timing advantage in primates

Abstract

Sensory systems across the brain are specialized for their input, yet some principles of neural organization are conserved across modalities. The pattern of anatomical connections from the primate auditory cortex to the temporal, parietal, and prefrontal lobes suggests a possible division into dorsal and ventral auditory processing streams, with the dorsal stream originating from more caudal areas of the auditory cortex, and the ventral stream originating from more rostral areas. These streams are hypothesized to be analogous to the well-established dorsal and ventral streams of visual processing. In the visual system, the dorsal processing stream shows substantially faster neural response latencies than does the ventral stream. However, the relative timing of putative dorsal and ventral stream processing has yet to be explored in other sensory modalities. Here, we compare distributions of neural response latencies from 10 different areas of macaque auditory cortex, confirmed by individual anatomical reconstructions, to determine whether a similar timing advantage is found for the hypothesized dorsal auditory stream. Across three varieties of auditory stimuli (clicks, noise, and pure tones), we find that latencies increase with hierarchical level, as predicted by anatomical connectivity. Critically, we also find a pronounced timing differential along the caudal-to-rostral axis within the same hierarchical level, with caudal (dorsal stream) latencies being faster than rostral (ventral stream) latencies. This observed timing differential mirrors that found for the dorsal stream of the visual system, suggestive of a common timing advantage for the dorsal stream across sensory modalities.systems neuroscience | neurophysiology | hierarchy

Selectivity for space and time in early areas of the auditory dorsal stream in the rhesus monkey

“…Higher spatial selectivity in CL than in CM has been shown previously for azimuth only (Miller and Recanzone 2009;Woods et al 2006). Camalier et al (2012) demonstrated particularly fast latencies in CM. A region representing spatial location of sounds is expected to be strongly linked to the visual system in order to relate sounds to visual objects in space; indeed, visual connections and projections from area 7a (which is involved in coding location of targets for reaching; Andersen 1997) are stronger in CL than in CM (Falchier et al 2010;Smiley et al 2007).…”

“…7, left). This indicates that CM receives auditory information not only from A1 ) but also from another, faster source, likely the anterodorsal nucleus of the medial geniculate body (MGB; Bartlett and Wang 2011;Camalier et al 2012;Hackett et al 2007).…”

“…Some authors have proposed that fast latencies may be beneficial for quick action selection performed by the dorsal stream, possibly under a threat (Camalier et al 2012;Jääskeläinen et al 2004). Alternatively, fast response latency may serve by producing an "initial guess" of object identity in the dorsal stream, subsequently utilized by the ventral stream for slower and more specific analysis, or by attentional mechanisms (Ahveninen et al 2006).…”

“…Locking to fast temporal modulations has been reported to be either poorer (Oshurkova et al 2008) or similar or better (Scott et al 2011) in CM compared with A1. Response latencies have been shown to be either similar in A1 and CM (Oshurkova et al 2008;Recanzone et al 2000b) or shorter in CM (Camalier et al 2012;Kajikawa et al 2005;Scott et al 2011).…”

“…This has rarely been the case; in many studies only one of these areas was investigated, areas were pooled together, or CM was studied in different animals from CL (Camalier et al 2012;Oshurkova et al 2008;Recanzone et al 2000a;Scott et al 2011;Tian et al 2001;Zhou and Wang 2012). So far, the two areas have been compared directly only in one set of monkeys, showing enhanced spatial selectivity in the horizontal plane in CL but not CM (Miller and Recanzone 2009;Woods et al 2006).…”