Predictive motor control of sensory dynamics in auditory active sensing

Abstract

Neuronal oscillations present potential physiological substrates for brain operations that require temporal prediction. We review this idea in the context of auditory perception. Using speech as an exemplar, we illustrate how hierarchically organized oscillations can be used to parse and encode complex input streams. We then consider the motor system as a major source of rhythms (temporal priors) in auditory processing, that act in concert with attention to sharpen sensory representations and link them across areas. We discuss the circuits that could mediate this audio-motor interaction, notably the potential role of the somatosensory system. Finally, we reposition temporal predictions in the context of internal models, discussing how they interact with feature-based or spatial predictions. We argue that complementary predictions interact synergistically according to the organizational principles of each sensory system, forming multidimensional filters crucial to perception.

Figure 1. Multiple time scales of speech and auditory brain rhythms

(A) Time-frequency decomposition of a sentence envelope (a 1/f detrending on the signal’s amplitude was applied for visualization purpose). (Upper inset) Sentence waveform and its corresponding envelope (black thick line). (Right inset) Modulation spectrum. (B) Time-frequency decomposition of the spontaneous activity recorded in the supragranular primary auditory cortex of an awake macaque monkey. (Upper inset) Current source density (CSD) raw data. (Right inset) Modulation spectrum. Adapted from [69]. (C) Relationship between excitability, as indexed by the action potential firing rate (red), and the phase of oscillation, as indexed by a local field potential (blue); neuronal oscillations have optimal (high excitability) and non-optimal (low excitability) phases. (D) Schematic highlighting the typical ‘nested’ nature of oscillations. The (top) green trace illustrates a typical recording of oscillations. The traces below illustrate the individual oscillatory components in the delta (1.5Hz), theta (7Hz) and low gamma (35Hz) bands that comprise the composite waveform. Hierarchically organized phase-amplitude coupling between frequencies is present. (C-D) Adapted from [14]. (E) From top to bottom: a. Low-frequency LFP, with phase angle color-coded. b. Binned LFP phase during 30 trials. c. Corresponding spike raster plot. d. Mean firing rate across trials: The colored bars indicate the typical phase at each peak. Gray lines mark pairs of peaks with similar mean firing rate but different phase angle. The two instances in each pair (e.g. a1, a2) can be distinguished based on LFP phase but not based on the firing rate. Adapted form [32].

Figure 2. Regional connections of auditory cortex in the macaque brain

(A) Topographic connections of belt/parabelt auditory areas with areas of prefrontal, posterior parietal, superior temporal, and visual cortex (red: rostral areas; blue: caudal areas). All connections are reciprocal. Line thickness denotes relative strength. Primary (core) areas (not shown) have extremely limited connections outside of auditory cortex. (B) Schematic diagram summarizing connections of belt/parabelt areas with sensory, multisensory, and motor areas. Note that connections between auditory and premotor/motor areas have not been established in primates, and are either weak or absent. (C) Schematic diagram of principal routes of information flow between major regions of cortex, basal ganglia, and thalamus. Corticostriatal projections from most areas are topographically organized and not reciprocal. (D) Summary of topographic projections from belt/parabelt auditory cortex to caudate and putamen. Topographical relationships indicated by color gradient. Primary (core) auditory cortex does not project to the striatum in primates, or projections are limited. Abbreviations: CB/CPB, caudal belt and parabelt; RB/RPB, rostral belt and parabelt; M1, primary motor cortex; S2, second somatosensory area; PV, parietoventral somatosensory area; Ri, retroinsular area; STGr, rostral superior temporal gyrus; TPO, temporal polysensory area; Tpt, temporal parietotemporal area; VIP, ventral intraparietal area; V1/V2, visual areas 1 and 2; ProS, area prostriata (visual); VA, ventral anterior nucleus; VL, ventral lateral nucleus; MD, medial dorsal nucleus; GP, globus pallidus; NB, nucleus basalis.

Figure 3

Summary of the average temporal patterns of MUA (blue) and the CSD-derived beta band power (red) in the supragranular layer of the second somatosensory area (S2) recorded from one monkey during performance of an audio-visual (AV) oddball task [70]. Although the monkey held a lever, a series of audiovisual stimuli were presented. Data are aligned to the onset (0 sec) of AV stimuli during the task. Stimuli were repeating 500 ms vocal movie clips (SOA = 1.4 sec; static-to-movie face) with random oddballs (20%) in which face or voice differed from the standard. Upon detection of an oddball, monkey released the lever for a reward. The black dashed line indicates the mean reaction times on the adjoining target trials. For each signal, mean and 95% confidence intervals are shown (n=16, bootstrap). Each signal was normalized by the standard deviation estimated from periods of −2 to 2 sec from the onset of stimuli. MUA was sampled at 2 kHz, CSD power was sampled at 0.5 kHz.

Figure 4. Auditory active sensing

(A) A forward model (corollary discharge/efference copy) predicts the sensory consequences of a movement based on the motor command. When a movement is self-produced, its sensory consequences can be accurately predicted and this prediction can be used to attenuate the sensory effects of the movement. Adapted from [71]. (B) Example of auditory active sensing paradigm. Participants listen to a sequence of pure tones and then estimate the average pitch of targets, while ignoring distractors. First row: rhythmic motor tracking in phase with the reference beat throughout the sequence. Second row: references indicating the beat. Third (fourth) rows: targets (distractors) presented in phase (antiphase) with the reference beat. Dark (light) grey lines indicate the temporal distance between the motor act and the onset of the target (distractor). Fifth row: sensory gains assigned to successive targets and distractors. The shorter the temporal distance between a tone and a motor act, the stronger the temporal prediction, and the higher the sensory gain assigned to the tone. Adapted from [10*].