In search of an auditory engram

Self Cite

A stimulus trace may be temporarily retained either actively [i.e., in working memory (WM)] or by the weaker mnemonic process we will call passive short-term memory, in which a given stimulus trace is highly susceptible to "overwriting" by a subsequent stimulus. It has been suggested that WM is the more robust process because it exploits long-term memory (i.e., a current stimulus activates a stored representation of that stimulus, which can then be actively maintained). Recent studies have suggested that monkeys may be unable to store acoustic signals in long-term memory, raising the possibility that they may therefore also lack auditory WM. To explore this possibility, we tested rhesus monkeys on a serial delayed match-to-sample (DMS) task using a small set of sounds presented with ∼1-s interstimulus delays. Performance was accurate whenever a match or a nonmatch stimulus followed the sample directly, but it fell precipitously if a single nonmatch stimulus intervened between sample and match. The steep drop in accuracy was found to be due not to passive decay of the sample's trace, but to retroactive interference from the intervening nonmatch stimulus. This "overwriting" effect was far greater than that observed previously in serial DMS with visual stimuli. The results, which accord with the notion that WM relies on long-term memory, indicate that monkeys perform serial DMS in audition remarkably poorly and that whatever success they had on this task depended largely, if not entirely, on the retention of stimulus traces in the passive form of shortterm memory.macaque | primate | vocalization W orking memory (WM) is a system that enables the temporary maintenance and manipulation of information necessary to guide behavior (1, 2). The term "working memory" has sometimes been applied to parametric sensory discriminations (3) [e.g., comparing the acoustic frequency of two successive tones, or the visual contrast of two successive images, separated by a short interstimulus interval (ISI)]. However, in the absence of the need for maintaining and manipulating the stimuli, such discriminations may be more properly described as tests of a type of shortterm memory (STM) that we will call passive short-term memory (pSTM) rather than WM.Definitions and models of WM vary (4), but the concepts of STM (particularly pSTM) and WM differ along a dimension of increasing attention to the stimulus item and greater reliance on its stored representation. Indeed, WM has been posited to differ from other forms of STM by operating not on a recently presented item, per se, but on the activation of a representation of that item stored in long-term memory (LTM) (4-7). This distinction is related to another, viz. the distinction between categorical perception and continuous, noncategorical perception, the former term implying that perception of some stimuli activates their previously stored representations sorted into categories on the basis of either their physical similarity or some more abstract factor. The capacity of WM in vision has b...

Section: Discussionmentioning

confidence: 63%

mentioning

confidence: 99%

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

Scott

Mishkin

Yin

2012

Self Cite

“…There are considerable anatomical data that the midventrolateral prefrontal cortex (and particularly area 45) is extensively connected with the superior temporal gyrus and the nearby dorsal bank of the superior temporal sulcus (through the extreme capsule and the arcuate fasciculus) and also with the inferior parietal lobule (area PG) (via the second branch of the superior longitudinal fasciculus) (14, 16-18, 20, 37). The superior temporal region of the primate brain is critical for the encoding and short-term maintenance of auditory information (32,33,38), whereas the caudal superior temporal gyrus and the adjacent parabelt region in the caudal superior temporal sulcus entering the inferior parietal lobule are involved in the spatial aspects of auditory coding (34,36). Indeed, a recent study using transcranial magnetic stimulation has shown that the caudal part of the superior temporal gyrus, close to the inferior parietal lobule, is involved in auditory localization to a greater extent than the more rostral temporal region (39).…”

Section: Discussionmentioning

confidence: 99%

Selective memory retrieval of auditory what and auditory where involves the ventrolateral prefrontal cortex

Kostopoulos

Petrides

2016

There is evidence from the visual, verbal, and tactile memory domains that the midventrolateral prefrontal cortex plays a critical role in the top-down modulation of activity within posterior cortical areas for the selective retrieval of specific aspects of a memorized experience, a functional process often referred to as active controlled retrieval. In the present functional neuroimaging study, we explore the neural bases of active retrieval for auditory nonverbal information, about which almost nothing is known. Human participants were scanned with functional magnetic resonance imaging (fMRI) in a task in which they were presented with short melodies from different locations in a simulated virtual acoustic environment within the scanner and were then instructed to retrieve selectively either the particular melody presented or its location. There were significant activity increases specifically within the midventrolateral prefrontal region during the selective retrieval of nonverbal auditory information. During the selective retrieval of information from auditory memory, the right midventrolateral prefrontal region increased its interaction with the auditory temporal region and the inferior parietal lobule in the right hemisphere. These findings provide evidence that the midventrolateral prefrontal cortical region interacts with specific posterior cortical areas in the human cerebral cortex for the selective retrieval of object and location features of an auditory memory experience.fMRI | prefrontal cortex | memory retrieval | auditory | control processes

“…† with this dual-tract system extending ventrally into the middle and inferior temporal gyri as well as dorsally into the ventral premotor gyrus. By comparison, the arcuate fasciculus in monkeys is a primitive one (7,8,11,62), providing a possible explanation for the monkey's apparent inability to store the representations of fluctuating acoustic stimuli in long-term memory (5). Conversely, the large size and complexity of this dual tract in humans may have enabled long-term memory for speech sounds by providing the auditory system with an input that transforms an intractable, fluctuating, acoustic stimulus into an integrated acoustic/oromotor sequence that can be stored for subsequent recognition.…”

Section: Discussionmentioning

confidence: 99%

“…In vision and touch, monkeys master the rule for one-trial recognition memory extremely rapidly, within several daily sessions (1,2); and once they have learned the rule, it can be shown that they have stimulus-retention thresholds (performance at 75% accuracy) of 10-20 min after viewing or palpating a novel stimulus for only 1-2 s (3,4). In audition, by contrast, monkeys acquire the rule for one-trial memory exceedingly slowly, requiring a full year or two of training before they can master it, if they succeed at all; and if they do succeed, their stimulus-retention thresholds are found to extend no longer than 30-40 s after stimulus presentation (5). This marked disparity in mnemonic ability across sensory modalities suggests that, in audition alone, monkeys seem unable to store stimulus representations in long-term memory (LTM) and, consequently, appear to be limited mnemonically to the time period covered by short-term memory.…”

mentioning

confidence: 99%

Test of a motor theory of long-term auditory memory

Schulze

Vargha‐Khadem

Mishkin

2012

Self Cite

Monkeys can easily form lasting central representations of visual and tactile stimuli, yet they seem unable to do the same with sounds. Humans, by contrast, are highly proficient in auditory long-term memory (LTM). These mnemonic differences within and between species raise the question of whether the human ability is supported in some way by speech and language, e.g., through subvocal reproduction of speech sounds and by covert verbal labeling of environmental stimuli. If so, the explanation could be that storing rapidly fluctuating acoustic signals requires assistance from the motor system, which is uniquely organized to chain-link rapid sequences. To test this hypothesis, we compared the ability of normal participants to recognize lists of stimuli that can be easily reproduced, labeled, or both (pseudowords, nonverbal sounds, and words, respectively) versus their ability to recognize a list of stimuli that can be reproduced or labeled only with great difficulty (reversed words, i.e., words played backward). Recognition scores after 5-min delays filled with articulatory-suppression tasks were relatively high (75-80% correct) for all sound types except reversed words; the latter yielded scores that were not far above chance (58% correct), even though these stimuli were discriminated nearly perfectly when presented as reversed-word pairs at short intrapair intervals. The combined results provide preliminary support for the hypothesis that participation of the oromotor system may be essential for laying down the memory of speech sounds and, indeed, that speech and auditory memory may be so critically dependent on each other that they had to coevolve.evolution | mimic | arcuate fasciculus T he proficiency with which monkeys perform tests of both visual and tactile recognition does not extend to auditory recognition. In vision and touch, monkeys master the rule for one-trial recognition memory extremely rapidly, within several daily sessions (1, 2); and once they have learned the rule, it can be shown that they have stimulus-retention thresholds (performance at 75% accuracy) of 10-20 min after viewing or palpating a novel stimulus for only 1-2 s (3, 4). In audition, by contrast, monkeys acquire the rule for one-trial memory exceedingly slowly, requiring a full year or two of training before they can master it, if they succeed at all; and if they do succeed, their stimulus-retention thresholds are found to extend no longer than 30-40 s after stimulus presentation (5). This marked disparity in mnemonic ability across sensory modalities suggests that, in audition alone, monkeys seem unable to store stimulus representations in long-term memory (LTM) and, consequently, appear to be limited mnemonically to the time period covered by short-term memory. Humans, on the other hand, are highly proficient at storing lasting representations of auditory stimuli, such as words and tunes, thereby enabling their later recognition. What accounts for these striking mnemonic differences between audition and other sensory modalities in...