Abstract

Important information from the environment often arrives to the brain in temporally extended sequences. Language, music, actions, and complex events generally unfold over time. When such informational sequences exceed the limited capacity of working memory, the human brain relies on its ability to accumulate information in long-term memory over several encounters with a complex stimulus. A longstanding question in psychology and neuroscience is whether the neural structures associated with working memory storage—often viewed as capacity limited and temporary—have any builtin ability to store information across longer temporal delays. According to the classic Hebbian dual memory theory, temporally local “activity traces” underlie immediate perception and working memory, whereas “structural traces” undergird long-term learning. Here we examine whether brain structures known to be involved in working maintenance of auditory sequences, such as area Spt, also show evidence of memory persistence across trials. We used representational similarity analysis (RSA) and the Hebb repetition paradigm with supracapacity tonal sequences to test whether repeated sequences have distinguishable multivoxel activity patterns in the auditory-motor networks of the brain. We found that, indeed, area Spt and other nodes of the auditory dorsal stream show multivoxel patterns for tone sequences that become gradually more distinct with repetition during working memory for supracapacity tone-sequences. The findings suggest that the structures are important for working memory are not “blank slates,” wiped clean from moment to moment, but rather encode information in a way can lead to cross-trial persistence.

Highlights

  • Humans are frequently faced with the need to detect, briefly store, and act upon a sequence of information encountered in the environment

  • In the current study we examined whether functional-anatomical structures that are known to be involved in auditory perception and short-term maintenance show evidence of long-term learning in a Hebb repetition paradigm with 9item tone sequences

  • We were most interested in examining whether Spt, a region that has repeatedly been implicated in tasks requiring the short-term maintenance of auditory-verbal and auditory-tonal sequences, operates as a pure “buffer” —wiping its contents clean from trial to trial— or whether we might detect evidence for the persistence of sequence-specific representations that spanned across trials

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Summary

Introduction

Humans are frequently faced with the need to detect, briefly store, and act upon a sequence of information encountered in the environment. A question that has long interested psychologists and neuroscientists has been how the brain holds on to new arbitrary sequences of information. The psychologist Donald Hebb was interested in the neurophysiological mechanisms (“a dual trace” theory) that underlie both the learning and short-term maintenance of sensory- or sensory-motor sequences of the kind exemplified by the phone-number task. Hebb conceived of two main physiological mechanisms that support short-term maintenance and long-term learning, respectively [1] He proposed that short-term maintenance of information is supported by activity traces encoded in distributed cell assemblies that could achieve temporary persistence through reverberatory activity that relied on sensory-motor connections and synaptic feedback loops. Hebb proposed that long-term learning was mediated by the repeated co-occurrence of synaptic connectivity among sets of neurons, leading to a gradual strengthening of connections—a structural trace—between such sets or assemblies

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