Neural correlates of short-term memory in primate auditory cortex

Abstract

Behaviorally-relevant sounds such as conspecific vocalizations are often available for only a brief amount of time; thus, goal-directed behavior frequently depends on auditory short-term memory (STM). Despite its ecological significance, the neural processes underlying auditory STM remain poorly understood. To investigate the role of the auditory cortex in STM, single- and multi-unit activity was recorded from the primary auditory cortex (A1) of two monkeys performing an auditory STM task using simple and complex sounds. Each trial consisted of a sample and test stimulus separated by a 5-s retention interval. A brief wait period followed the test stimulus, after which subjects pressed a button if the sounds were identical (match trials) or withheld button presses if they were different (non-match trials). A number of units exhibited significant changes in firing rate for portions of the retention interval, although these changes were rarely sustained. Instead, they were most frequently observed during the early and late portions of the retention interval, with inhibition being observed more frequently than excitation. At the population level, responses elicited on match trials were briefly suppressed early in the sound period relative to non-match trials. However, during the latter portion of the sound, firing rates increased significantly for match trials and remained elevated throughout the wait period. Related patterns of activity were observed in prior experiments from our lab in the dorsal temporal pole (dTP) and prefrontal cortex (PFC) of the same animals. The data suggest that early match suppression occurs in both A1 and the dTP, whereas later match enhancement occurs first in the PFC, followed by A1 and later in dTP. Because match enhancement occurs first in the PFC, we speculate that enhancement observed in A1 and dTP may reflect top–down feedback. Overall, our findings suggest that A1 forms part of the larger neural system recruited during auditory STM.

Neural Correlates of Auditory Short-Term Memory in Rostral Superior Temporal Cortex

“…2), but delay activity was seldom selective for the preceding stimulus. Similar results have been reported in the caudal belt [23], dorsal temporal pole (our TGd; [28]), and recently in AI [29]. Our serial DMS paradigm revealed that while DS persisted throughout the trial, DE was not robust to interference, and diminished in tandem with behavioral accuracy (Fig.…”

“…The ME that we observed, which appeared 80-180 ms after stimulus onset, has not been described previously in auditory cortex; ME ≥300 ms after sound onset has been reported in AI and TGd [28, 29], but likely represents response selection and/or feedback from PFC [13]. By contrast, short-latency MS has been reported in AI (23% of units;[29]), caudal auditory belt (22%;[23]), and TGd (9%; [28]). Collectively these data argue against a specialization for STM at the temporal pole, and in favor of a more distributed representation that includes core and belt.…”

“…Delay suppression is seldom mentioned in the visual DMS literature, but common in primate studies of auditory STM [13, 23, 28, 29]. Inhibitory projections from PFC to the STGr [30] provide a possible substrate for the robust DS observed in our unit data (Fig.…”

Auditory short-term memory in the primate auditory cortex

“…Recent studies have re-opened the question of how cortical neurons represent auditory STM in the nonhuman primate model (Fig 2; Bigelow et al, 2014; Ng et al, 2014; Plakke et al, 2013; Scott et al, 2014). As described above (section 2.2), Scott et al (2012; 2012; 2014) applied a serial DMS paradigm using stimuli and delays of a similar duration to those of Gottlieb et al (1989) but with two key differences: stimuli comprised a range of acoustic categories, and intervening nonmatch stimuli could appear between the sample and match (Fig.…”

“…Part of the recorded region was co-extensive with the rostral superior temporal gyrus lesion applied by Fritz et al (2005; see section 2.1), which reduced forgetting thresholds from 30–50 s to <10 s, implicating this region in supporting auditory DMS. A complementary set of studies from Poremba and colleagues recorded from areas bracketing the rSTC at lower and higher stages of cortical processing: the primary auditory cortex (AI; Bigelow et al, 2014), and the dorsal temporal pole (dTP: Ng et al, 2014), as well as the dorsolateral PFC (Plakke et al, 2013). The following sections (3.1–3.3) integrate these findings to outline a temporal-frontal network engaged during auditory STM in the nonhuman primate.…”