Persistent neural activity in auditory cortex is related to auditory working memory in humans and nonhuman primates

Huang, Ying; Matysiak, Artur; Heil, Peter; König, Reinhard; Brosch, Michael

doi:10.7554/elife.15441

Cited by 54 publications

(53 citation statements)

References 70 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Sustained maintenance activation has now been observed across multiple brain regions in tasks involving various sensory modalities (Bashivan et al, 2014a;Masse et al, 2020;Salazar et al, 2012; but see Yue et al, 2019). In agreement with prior neuroimaging studies on WM (Grimault et al, 2014;Huang et al, 2016;Vogel and Machizawa, 2004), we similarly find that sustained EEG activity during WM maintenance is modulated by stimulus load. Our results corroborate fMRI findings (Kumar et al, 2016) by confirming, electrophysiologically, that successful auditory WM depends on elevated activity within AC and adjacent auditory cortex.…”

Section: Discussionsupporting

confidence: 89%

“…Some reports show enhancements (Gaab et al, 2003a;Grimault et al, 2009;Kumar et al, 2016) and others suppression (Linke et al, 2011;Zatorre et al, 1994) of auditory cortical responses with memory load. ERP studies are similarly ambiguous with studies showing a decrease (Golob and Starr, 2000;Pratt et al, 1989) or increase (Alain et al, 2009;Grimault et al, 2014;Huang et al, 2016;Lefebvre et al, 2013;Vogel and Machizawa, 2004) in late (> 400 ms) slow wave potentials with load level. On the contrary, direct unit recordings from animals suggest AC neurons can actually show both suppression and enhancement effects according to the mnemonic context of sounds (Scott et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…In fact, few studies have examined the neurophysiological correlates of auditory WM. A persistent and dominant view, adopted from the visual sciences, is that regions beyond auditory cortex (AC) drive WM in human and non-human primates (Gaab et al, 2003b;Grady et al, 2008;Huang et al, 2016;Kumar et al, 2016;Lefebvre et al, 2013;Mencarelli et al, 2019). In this framework, AC is responsible mainly for precise encoding of stimulus representations rather than the active maintenance of information in a memory buffer.…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Auditory cortex supports verbal working memory capacity

Bidelman

Brown

Bashivan

2020

Preprint

View full text Add to dashboard Cite

Working memory (WM) is a fundamental construct of human cognition that predicts important faculties such as language abilities and scholastic achievement. The neural basis of auditory WM is thought to reflect a distributed brain network consisting of canonical memory and central executive brain regions including frontal lobe, prefrontal areas, and hippocampus. Yet, the role of auditory (sensory) cortex in supporting active memory representations remains controversial. Here, we recorded neuroelectric activity via EEG as listeners actively performed an auditory version of the Sternberg memory task. Memory load was taxed by parametrically manipulating the number of auditory tokens (letter sounds) held in memory. Source analysis of scalp potentials showed that sustained neural activity maintained in auditory cortex (AC) prior to memory retrieval closely scaled with behavioral performance. Brain-behavior correlations revealed lateralized modulations in left (but not right) AC predicted individual differences in auditory WM capacity. Our findings confirm a prominent role of auditory cortex, traditionally viewed as a sensory-perceptual processor, in actively maintaining memory traces and dictating individual differences in behavioral WM limits.

show abstract

Section: Discussionsupporting

confidence: 89%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Auditory cortex supports verbal working memory capacity

Bidelman

Brown

Bashivan

2020

Preprint

View full text Add to dashboard Cite

show abstract

“…Recent studies have shown that delay activity in the auditory cortex reflects the content of auditory WM (Huang et al, 2016;Kumar et al, 2016;Uluç et al, 2018). Thus, similar to visual WM maintenance, which has been found to result in content-specific delay-activity in the visual cortex (Harrison & Tong, 2009), auditory WM content is also maintained in a network that recruits the same brain area responsible for sensory processing.…”

Section: Discussionmentioning

confidence: 89%

“…Previous research has relied on testing whether sensory cortices exhibit content-specific neural activity during maintenance. While this has indeed been shown for visual memories in occipital areas (e.g., Harrison & Tong, 2009) and, more recently, for auditory memories in the auditory cortex (Huang, Matysiak, Heil, König, & Brosch, 2016;Kumar et al, 2016;Uluç, Schmidt, Wu, & Blankenburg, 2018), WM-specific activity in the sensory cortex is not always present (Bettencourt & Xu, 2016), fuelling an ongoing debate over whether sensory cortices are necessary for WM maintenance (Scimeca, Kiyonaga, & D'Esposito, 2018;Xu, 2017). However, the neural WM network may not be solely based on measurable neural activity, and it has been proposed that information in WM may be maintained in an "activity-silent" network (Stokes, 2015) -for example, changes in short-term connectivity (Mongillo, Barak, & Tsodyks, 2008).…”

Section: Introductionmentioning

confidence: 78%

Impulse responses reveal unimodal and bimodal access to visual and auditory working memory

Wolff

Kandemir

Stokes³

et al. 2019

Preprint

View full text Add to dashboard Cite

It is unclear to what extent sensory processing areas are involved in the maintenance of sensory information in working memory (WM). Previous studies have thus far relied on finding neural activity in the corresponding sensory cortices, neglecting potential activitysilent mechanisms such as connectivity-dependent encoding. It has recently been found that visual stimulation during visual WM maintenance reveals WM-dependent changes through a bottom-up neural response. Here, we test whether this impulse response is uniquely visual and sensory-specific. Human participants (both sexes) completed visual and auditory WM tasks while electroencephalography was recorded. During the maintenance period, the WM network was perturbed serially with fixed and task-neutral auditory and visual stimuli. We show that a neutral auditory impulse-stimulus presented during the maintenance of a pure tone resulted in a WM-dependent neural response, providing evidence for the auditory counterpart to the visual WM findings reported previously. Interestingly, visual stimulation also resulted in an auditory WM-dependent impulse response, implicating the visual cortex in the maintenance of auditory information, either directly, or indirectly as a pathway to the neural auditory WM representations elsewhere. In contrast, during visual WM maintenance only the impulse response to visual stimulation was content-specific, suggesting that visual information is maintained in a sensory-specific neural network, separated from auditory processing areas. Significance StatementWorking memory is a crucial component of intelligent, adaptive behaviour. Our understanding of the neural mechanisms that support it has recently shifted: rather than being dependent on an unbroken chain of neural activity, working memory may rely on transient changes in neuronal connectivity, which can be maintained efficiently in activity-silent brain states. Previous work using a visual impulse stimulus to perturb the memory network has implicated such silent states in the retention of line orientations in visual working memory. Here, we show that auditory working memory similarly retains auditory information. We also observed a sensory-specific impulse response in visual working memory, while auditory memory responded bi-modally to both visual and auditory impulses, possibly reflecting visual dominance of working memory.

show abstract

Auditory cortex modelled as a dynamical network of oscillators: understanding event-related fields and their adaptation

et al. 2022

Self Cite

View full text Add to dashboard Cite

Adaptation, the reduction of neuronal responses by repetitive stimulation, is a ubiquitous feature of auditory cortex (AC). It is not clear what causes adaptation, but short-term synaptic depression (STSD) is a potential candidate for the underlying mechanism. In such a case, adaptation can be directly linked with the way AC produces context-sensitive responses such as mismatch negativity and stimulus-specific adaptation observed on the single-unit level. We examined this hypothesis via a computational model based on AC anatomy, which includes serially connected core, belt, and parabelt areas. The model replicates the event-related field (ERF) of the magnetoencephalogram as well as ERF adaptation. The model dynamics are described by excitatory and inhibitory state variables of cell populations, with the excitatory connections modulated by STSD. We analysed the system dynamics by linearising the firing rates and solving the STSD equation using time-scale separation. This allows for characterisation of AC dynamics as a superposition of damped harmonic oscillators, so-called normal modes. We show that repetition suppression of the N1m is due to a mixture of causes, with stimulus repetition modifying both the amplitudes and the frequencies of the normal modes. In this view, adaptation results from a complete reorganisation of AC dynamics rather than a reduction of activity in discrete sources. Further, both the network structure and the balance between excitation and inhibition contribute significantly to the rate with which AC recovers from adaptation. This lifetime of adaptation is longer in the belt and parabelt than in the core area, despite the time constants of STSD being spatially homogeneous. Finally, we critically evaluate the use of a single exponential function to describe recovery from adaptation.

show abstract

Persistent neural activity in auditory cortex is related to auditory working memory in humans and nonhuman primates

Cited by 54 publications

References 70 publications

Auditory cortex supports verbal working memory capacity

Auditory cortex supports verbal working memory capacity

Impulse responses reveal unimodal and bimodal access to visual and auditory working memory

Auditory cortex modelled as a dynamical network of oscillators: understanding event-related fields and their adaptation

Contact Info

Product

Resources

About