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

Abstract

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.

Understanding rostral–caudal auditory cortex contributions to auditory perception

“…1b). This rostral–caudal organization is also seen in the connections between the auditory thalamus and the rostral and caudal core auditory fields; caudal core field A1 and the rostral auditory core field (R) both receive the vast majority of their inputs from the ventral medial geniculate body, whereas the rostral-most core field, the rostral temporal core field (RT), receives a greater proportion of inputs from the posterodorsal medial geniculate body13 (Fig. 1a).…”

“…Differences in the temporal response characteristics of the rostral and caudal auditory cortex have been reported in non-human primates over the past decade25,26. More recently, the rostral–caudal connectivity of the auditory cortex has been further elaborated12,13, and we have begun to see different temporal response characteristics to sound in the human brain31. Perhaps because of the extreme salience of heard speech as a vehicle for linguistic and social communication, or perhaps because of the clear clinical need to understand aphasia, cognitive neuroscience has often approached the understanding of the auditory cortex in a manner that has been largely focused on spoken language2.…”

“…Rostral–caudal differences extend into the thalamo-cortical connectivity of the rostral belt and parabelt areas. The rostrotemporal polar belt area (RTp), lying directly rostral to RT, receives most of its inputs from the posterodorsal, ventral and medial fields within the medial geniculate body, whereas the rostral superior temporal gyrus (STGr), lying lateral to RTp in the parabelt, is more strongly connected to the medial pulvinar and suprageniculate (Sg)–limitans (Lim) complex13.…”

“…This rostral–caudal organization of anatomy and connectivity has been taken as contributing evidence to support the idea that the nature of processing in the rostral and caudal auditory cortex may be qualitatively distinct. For instance, it has been suggested that rostral projections and fields may be more likely (than caudal projections) to play a fundamental role in the integration of audiovisual information because they are more strongly anatomically connected to thalamic nuclei that process visual information as well as sound13 (the medial pulvinar and Sg and Lim thalamic nuclei; Fig. 1a).…”

Top-down, contextual entrainment of neuronal oscillations in the auditory thalamocortical circuit

“…One possibility is that oscillations in high-frequency regions provide cyclic inhibition to low-frequency regions, thereby parsing the information contained in the stream of lower-frequency acoustic elements, like the role our results suggest for the pulvinar. The anatomical backdrop for this similarity might be direct medial pulvinar–A1 connectivity, which thus far has been demonstrated only for caudal A1 regions tuned to higher frequencies ( 78 ).…”