Distributed networks for auditory memory contribute differentially to recall precision

The representations held in working memory are inherently noisy, but attention directed to relevant objects can effectively enhance their fidelity. While recent working memory models suggest that memory representations are distributed across sensory and cognitive-control brain regions, it remains unknown how multiple brain networks generate this attentional gain in fidelity. Here, we investigated the contributions of the distinct brain networks in maintaining and enhancing memory representations using psychophysical modeling and fMRI. Human listeners performed an auditory syllable pitch-discrimination task, in which they received valid (vs. neutral) retro-active cues to selectively attend to one of the two syllable categories maintained in memory. Valid (vs. neutral) retro-cues facilitated task performance, eliciting faster recall and enhanced recall precision of syllables in memory. Valid retro-cues also led to increased neural activation in fronto-parietal and cingulo-opercular networks, but not in sensory-specific superior temporal cortex. Multivariate pattern analysis as a proxy for representational fidelity in memory revealed that attended syllable objects were maintained in distributed areas across superior temporal, frontal, parietal, and sensorimotor brain areas. However, neural fidelity in left superior temporal sulcus and its enhancement through attention-to-memory best predicted the ensuing individual gain in recall precision of auditory objects from memory. These results demonstrate that maintaining versus attentionally enhancing auditory memory representations are functionally separable mechanisms across distributed brain regions. Significance Statement Working memory is distributed across sensory and cognitive-control brain regions. But how do these brain networks enhance working memory precision when attention is re-directed to memory? We here investigate the contributions of distinct brain networks in maintaining and enhancing auditory memory representations through attention-to-memory using fMRI. We demonstrate that re-directing attention to the relevant auditory memory objects mainly recruits higher-order cognitive-control networks. Among the multiple brain regions retaining memory representations, however, attentional enhancement of the neural fidelity in superior temporal sulcus best predicts the individual gain in recall precision of auditory objects from memory. This study provides evidence of the interplay among the discrete, functionally specialized brain regions in maintaining and attentionally enhancing working memory representations. Lim et al. · Page 3 of 36 Introduction Working memory is a short-term mental storage that maintains perceptual information even in the absence of sensory input. A hallmark of working memory is in its limited capacity—that is, perceptual information held in memory are inherently imprecise and noisy (e.g., Cowan, 2001; Bays and Husain, 2008; Luck and Vogel, 2013; Ma et al., 2014). Selective attention thus plays a crucial role in overcoming the bottleneck of the limited capacity. Directing attention to the relevant information in memory can reduce inherent noise and enhance representations of the attended memory items—a process referred as retrospective attention (Griffin and Nobre, 2003; Postle, 2006; Gazzaley and Nobre, 2012; Serences and Kastner, 2014; Myers et al., 2017). However, the neural processes that pose a neural substrate of the behavioral benefit from retrospective attention remains unclear. Research on the neural bases of working memory and selective attention implicates that multiple functional brain networks support active maintenance of the attended memory items. Neuroimaging research across various modalities suggests that both domain-general networks related to attention (i.e., fronto-parietal network) and cognitive control (i.e., cinguloopercular network), and the sensory-specific neural regions are involved in maintaining items held in working memory (e.g., Goldman-Rakic, 1995; Harrison and Tong, 2009; Higo et al., 2011; Riggall and Postle, 2012; Kiyonaga and Egner, 2013; D'Esposito and Postle, 2015; Ester et al., 2015). For example, auditory and verbal working memory research demonstrated contributions of the domain-general networks and language-related brain regions (e.g., the inferior/middle frontal and premotor regions; (Baddeley, 2003; Hickok and Poeppel, 2007; Hickok, 2009; Koelsch et al., 2009; Fedorenko et al., 2011), and the bilateral auditory cortices retaining stimulus-specific features of the auditory information held in memory (Linke et al., 2011; Linke and Cusack, 2015; Kumar et al., 2016). Collectively, the converging evidence suggests that neural traces of memory representations under focused attention are maintained across distributed brain networks. However, we do not know whether and how the discrete networks support the neural enhancement from attention directed to memory. In particular, how do these large-scale brain networks support retrospective attention leading to enhancement? How do the memory representations maintained in these brain networks directly affect the attentional gain in improving the mnemonic fidelity? These questions are especially important in understanding auditory memory representations as selective attention plays a crucial role in maintaining precise auditory objects in memory while suppressing irrelevant noise often intermixed with task-relevant acoustic signals (Fritz et al., 2007; Shinn-Cunningham, 2008; Wilsch and Obleser, 2016). Lim et al. · Page 4 of 36 Prior auditory working memory work has demonstrated that retrospective attention enhances representational precision of the attended versus unattended objects held in memory (Lim et al., 2015; 2018). Importantly, such precision benefit has been reflected in EEG neural signatures (i.e., enhanced sustained negativity and neural alpha (~10 Hz) oscillatory power), indicating that greater cognitive resource is allocated to the attended memory object, which ultimately enhances its representational precision (Lim et al., 2015). However, the limited spatial resolution of EEG cannot delineate how distinct brain networks— cognitive control vs. auditory processing regions—contribute to precision benefit from retrospective attention. To investigate the neural underpinning of retrospective attentional gain in mnemonic fidelity, we conducted an fMRI experiment, in which participants performed a previously established auditory working memory task—a delayed recall of syllable pitch discrimination task (Lim et al., 2015; 2018; Alavash et al., 2018). In this task, listeners encoded two speech syllables into memory, and received one of the two types of retroactive cues that either directed attention to one of the syllable objects or indicated to maintain both syllables in memory. So how should neural activities in domain-general and modality-specific brain regions be modulated when selective attention is re-directed to memory? Here, we used a multivariate classifier approach and fMRI data to quantify whether the memory representations were retained in aforementioned brain regions, and which of these brain regions contribute to the attentional gain in mnemonic fidelity. Given the existing controversy regarding whether different brain regions retain abstracted information versus stimulus-specific details in working memory (Christophel et al., 2012; Lee et al., 2013; Ester et al., 2015; Christophel et al., 2017; Long and Kuhl, 2018), we expected that the domain-general cognitive control and sensoryspecific brain regions would be differentially related to the benefits when attention is directed to objects maintained in memory. Our results demonstrate that selective attention to auditory memory leads to increased neural activity in domain-general cognitive control networks, but not in the auditory-sensitive superior temporal cortex. Using a multivariate analysis approach, we further show that while the neural representation of the attended memory object is distributed across the brain, these regions differentially contribute to the attentional gain in improving representational fidelity. The neural fidelity and its enhancement through attention-to-memory in left superior temporal sulcus and frontal cortex, but not in parietal cortex, are shown to predict the ensuing individual gain in recall precision of auditory objects from memory. Lim et al. · Page 5 of 36 Materials and Methods Participants Twenty-two participants (mean age: 27.9 years; SD: 2.75 years; age range: 25–35; 12 females) took part in the experiment that has been a part of a previously published study (Alavash et al., 2018). Participants were recruited from the participant database of the Max Planck Institute for Human Cognitive and Brain Sciences (Leipzig, Germany). Two additional participants underwent the study, but were excluded from the all data analyses due to excessive head movements (>5 mm). All subjects reported normal hearing, and no history of neurological or psychiatric disorders. None of the participants were under medication. All participants except one were right handed. All participants gave their informed written consent, and received financial compensation for their participation. The study procedure was in accordance with the Declaration of Helsinki. The local ethics committee (University of Leipzig) approved the study. Stimuli The stimulus material was identical to the ones used in previously published studies (Lim et al., 2015; 2018; Alavash et al., 2018). In brief, we used two German syllables, /da/ and /ge/. Each syllable category consisted of six naturally spoken tokens, truncated from German words recorded by a trained female speaker. All sound tokens were digitized at 44.1 kHz, and 200ms in duration. For each token, 3-ms and 30-ms linear ramps were applied at sound onset and offset, respectively. For each syllable category, two tokens served as to-be-probed syllables in t