Sound-identity processing in early areas of the auditory ventral stream in the macaque

Abstract

Auditory cortical processing is thought to be accomplished along two processing streams. The existence of a posterior/dorsal stream dealing, among others, with the processing of spatial aspects of sound has been corroborated by numerous studies in several species. An anterior/ventral stream for the processing of nonspatial sound qualities, including the identification of sounds such as species-specific vocalizations, has also received much support. Originally discovered in anterolateral belt cortex, most recent work on the anterior/ventral pathway has been performed on far anterior superior temporal (ST) areas and on ventrolateral prefrontal cortex (VLPFC). Regions of the anterior/ventral stream near its origin in early auditory areas have been less explored. In the present study, we examined three early auditory regions with different anteroposterior locations (caudal, middle, and rostral) in awake rhesus macaques. We analyzed how well classification based on sound-evoked activity patterns of neuronal populations replicates the original stimulus categories. Of the three regions, the rostral region (rR), which included core area R and medial belt area RM, yielded the greatest classification success across all stimulus classes or between classes of natural sounds. Starting from ∼80 ms past stimulus onset, clustering based on the population response in rR became clearly more successful than clustering based on responses from any other region. Our study demonstrates that specialization for sound-identity processing can be found very early in the auditory ventral stream. Furthermore, the fact that this processing develops over time can shed light on underlying mechanisms. Finally, we show that population analysis is a more sensitive method for revealing functional specialization than conventional types of analysis.

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

“…Data from a 20-ms pretrial period preceding the stimulus onset are shown on left, followed by "stimulus" data from 8 consecutive 20-ms time bins covering 0 -160 ms of stimulus. Double circles denote classification success that was significantly higher (P Ͻ 0.05) than pretrial classification success; filled circles represent stimulus classification success outside the reference range (P Ͻ 0.05; see Kuśmierek et al 2012). Dashed lines show boundaries of the reference range estimated by randomly reassigning the neurons to regions and repeating the k-means analysis in an identical way.…”

“…Most analysis methods are similar to those published recently (Kuśmierek et al 2012;Kuśmierek and Rauschecker 2009). Data from monkeys B and (partially) N were also used previously in population analyses of the rostral auditory areas (Kuśmierek et al 2012).…”

“…Two classes of natural stimuli (14 total) were also used to assess selectivity for natural sounds: seven monkey calls (MC) and seven environmental sounds (ES). Duration of PT and BPN stimuli was 300 ms, while MC and ES ranged between 150 and 1,706 ms (Kuśmierek et al 2012). ES were recorded in our animal facility and were therefore likely familiar and meaningful to the monkeys.…”

“…Linear discriminator analysis was performed as described previously (see Kuśmierek et al 2012;Kuśmierek and Rauschecker 2009;Recanzone 2008;Russ et al 2008 for details). For each unit and each stimulus class (PT, 1 ⁄3-octave BPN, 1-octave BPN, MC, and ES) we determined whether a single trial's spike train was more similar to combined remaining single spike trains elicited by the same stimulus (success) or to combined spike trains elicited by any other stimulus (failure).…”

“…We analyzed the ability of neural populations in the three areas to discriminate between four a priori sound categories: low-frequency artificial sounds, high-frequency artificial sounds, MC, and ES. The method was described previously (Kuśmierek et al 2012). Briefly, average firing rate for each neuron and stimulus was determined in eight 20-ms time bins covering the first 160 ms of the stimulus time and in a 20-ms bin preceding the stimulus (pretrial).…”