Primate auditory recognition memory performance varies with sound type

Abstract

Neural correlates of auditory processing, including for species-specific vocalizations that convey biological and ethological significance (e.g. social status, kinship, environment),have been identified in a wide variety of areas including the temporal and frontal cortices. However, few studies elucidate how non-human primates interact with these vocalization signals when they are challenged by tasks requiring auditory discrimination, recognition, and/or memory. The present study employs a delayed matching-to-sample task with auditory stimuli to examine auditory memory performance of rhesus macaques (Macaca mulatta), wherein two sounds are determined to be the same or different. Rhesus macaques seem to have relatively poor short-term memory with auditory stimuli, and we examine if particular sound types are more favorable for memory performance. Experiment 1 suggests memory performance with vocalization sound types (particularly monkey), are significantly better than when using non-vocalization sound types, and male monkeys outperform female monkeys overall. Experiment 2, controlling for number of sound exemplars and presentation pairings across types, replicates Experiment 1, demonstrating better performance or decreased response latencies, depending on trial type, to species-specific monkey vocalizations. The findings cannot be explained by acoustic differences between monkey vocalizations and the other sound types, suggesting the biological, and/or ethological meaning of these sounds are more effective for auditory memory. KeywordsMacaca mulatta; delayed matching-to-sample; vocalizations; performance; same; different; rhesus; monkey Monkeys have difficulty in learning a delayed matching-to-sample (DMTS) task requiring decisions about whether sounds match or not across memory delays (D'Amato and Colombo, 1985;Wright, 1998Wright, , 1999Fritz et al., 2005). Rhesus monkeys generally learn the rule for visual and tactile versions of this trial-unique delayed matching-and nonmatching-to-sample at short delays, within a few hundred trials (Murray and Mishkin, 1998;Buffalo et al., 1999;Zola et al., 2000), while a similar task, using auditory stimuli, takes them on average 15,000 trials to learn the rule at 5-second memory delays (Fritz et al., 2005). Auditory memory performance seems rather poor compared to using visual and tactile stimuli in similar tasks. Corresponding author and postal address for all authors: Amy Poremba, Ph.D., University of Iowa, E11 Seashore Hall, Department of Psychology, Iowa City, IA 52242, USA, amy-poremba@uiowa.edu, Office: 319-335-0372; Fax: 319-335-0191. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the conte...

Monkeys have a limited form of short-term memory in audition

“…A recent study of nonserial auditory DMS in rhesus monkeys by Ng et al (30) reported better performance and faster reaction times for conspecific vocalizations relative to other sound categories (similar to the categories used here) at delays of 5 s. In contrast, as shown in Fig. 3, our results indicate slightly better performance for tonal stimuli compared with all others, including monkey vocalizations.…”

Processing of communication sounds: Contributions of learning, memory, and experience

“…Similarly, European starlings are capable of learning to recognize pitch-shifted conspecific songs, but not pitch-shifted piano melodies (Bregman et al, 2012). A mnemonic advantage for CVs has also been reported in two recent studies of auditory short-term memory in humans (Weiss et al, 2012) and non-human primates (Ng et al, 2009). …”

“…However, these possibilities should be considered and tested when possible. On the plus side, there are several studies showing that different types of sounds in non-human primates elicit different behavioral and neural responses (Poremba et al, 2004; Ng et al, 2009), but future controlled testing of sounds with a similar frequency range to vocalizations and consideration of the amount of experience with the sounds will need further consideration. In addition, we must study whether the neural processes underlying associative conditioning also underlie learning of CVs and the relationship between conditioning, experience, and memory encoding.…”

Neural correlates of auditory recognition memory in primate lateral prefrontal cortex

“…Each sound stimulus, 220 to 500 ms (ms) long, was digitized and processed with a sampling frequency of 44,100 Hz and consisted of 8-bit monorecorded sound clips. A collection of 96 standard stimuli was used and classified into eight sound types similar in manner to Ng et al (2009). Animal vocalizations (n = 12) included sounds recorded from birds and domestic animals (e.g., cat and dog).…”

“…Each animal was trained on the DMS task with auditory stimuli as described in Ng et al (2009). The task employed go/no-go response rules for the auditory DMS task (Fig.…”