Skip to main content

Temporal predictions in the auditory cortex: neural mechanisms and their specificity across species and stimulus domains

Periodic Reporting for period 1 - BrainPredictDynamics (Temporal predictions in the auditory cortex: neural mechanisms and their specificity across species and stimulus domains)

Reporting period: 2018-09-01 to 2020-08-31

A recent paradigm shift in neuroscience has brought a substantial change in the way we see the brain. Instead of viewing it as an immensely complex input-output transformation organ, there is a growing consensus that its overarching function is to predict its immediate environment and minimise surprise. While the implementation of predictive processing in the brain is still being elucidated, a key challenge is to provide a unifying mechanistic explanation of neural expectations ranging from microscopic single-cell physiology, via models of interacting populations of neurons, to macroscopic signals observed non-invasively. To ground the theoretical claims that prediction propagation is a general principle of brain function, we need to understand the commonalities and boundary conditions of expectation signals across species, multiple domains (e.g. expectations of content, timing, location), and levels of complexity, from basic sensory processing to higher cognition.
Temporal predictions, in particular, are a current frontier in investigating the predictive brain capacities. While the importance of timing in perception was early recognised as a key determinant of behaviour, only recently has it been brought back to the centre of neuroscience. Auditory and speech perception are the optimal testing ground for studying temporal dynamics of predictive processing in the brain, as most auditory signals only gain meaning as temporal sequences. Thus, the current project will address two key challenges: (1) to test competing theories of temporal expectation mechanisms in the auditory cortex, using invasive electrophysiology in rodents and non-invasive human neuroimaging, and (2) to establish whether basic mechanisms observed in rodents and humans generalise across stimulus domains, from simple acoustic tones to complex hierarchical speech signals.
(1) Analysis of the neural correlates of temporal predictions in non-invasive recordings in humans (researchers involved: Ryszard Auksztulewicz, Jan Schnupp, Anna Christina Nobre) - results published as a journal article in Journal of Neuroscience (see figure attached)
(2) Analysis of the neural correlates of temporal predictions in direct, in vivo microelectrode recordings from auditory cortex in rats – neural omission responses to acoustic noise bursts presented at isochronous rates (researchers involved: Ryszard Auksztulewicz, Vani Rajendran, Nicol Harper, Jan Schnupp) – results presented at Society for Neuroscience 2019
(3) Mapping and quantification of the regional specificity of neural signatures of content-based predictions along the auditory cortical hierarchy, using in vivo microelectrode recordings from auditory cortex in rats – oddball responses to multiple acoustic features presented at isochronous rates (researchers involved: HyuJung An, Ryszard Auksztulewicz, HiJee Kang, Jan Schnupp) – results presented at Society for Neuroscience 2019 and published as a journal article in Hearing Research
(4) Mapping and quantification of the regional specificity of neural signatures of content-based predictions along the auditory cortical hierarchy using non-invasive electroencephalographic recordings in humans – oddball responses to multiple acoustic features presented at isochronous rates (researchers involved: HyunJung An, Ryszard Auksztulewicz, Kelvin Shing, Jan Schnupp) – manuscript in preparation
(5) Experimental design and data acquisition for the test whether activity and/or gain of single neurons in the central auditory system encodes predictions of stimulus timing and contents - using single-neuron optical imaging from multiple brain regions in mice (researchers involved: HyuJung An, Ryszard Auksztulewicz, HiJee Kang, Patrick Kanold, Jan Schnupp) - data analysis in progress
(6) Experimental design and data acquisition for assessing the extent to which stimulus-specific adaptation (SSA) is modulated by predictions of stimulus timing in higher-order cortex - using wide-field optical imaging from multiple brain regions in mice (researchers involved: HyuJung An, Ryszard Auksztulewicz, HiJee Kang, Patrick Kanold, Jan Schnupp) - data analysis in progress
Going beyond the state of the art, we have identified neural prediction errors to stimulus omissions at predictable moments in time - these neural prediction errors could be measured in the auditory cortex in anaesthetised rats, suggesting that the neural correlates of temporal predictions generalise across species and wakefulness states.
We have also identified differences in neural encoding of prediction errors depending on which acoustic feature is violated - these differences are largely consistent across species (rats and humans), and pinpoint to encoding of different prediction errors by distributed neural activity.
Initial analysis of optical imaging of neural activity in awake rodents showed that content-based prediction errors are additionally modulated by temporal predictions. The extent and mechanisms of these modulations are subject to an ongoing analysis.
In the last phase of the project, beyond completing the analyses described below, we will test whether temporal predictions at different hierarchical scales modulate speech processing in healthy human volunteers. This research will answer fundamental question about the neural mechanisms of temporal predictions.