Macaque monkeys and humans sample temporal regularities in the acoustic environment.

Many animal species show comparable abilities to detect basic rhythms and produce rhythmic behavior. Yet, the capacities to process complex rhythms and synchronize rhythmic behavior appear to be species-specific: vocal learning animals can, but some primates might not. This discrepancy is of high interest as there is a putative link between rhythm processing and the development of sophisticated sensorimotor behavior in humans. Do our closest ancestors show comparable endogenous dispositions to sample the acoustic environment in the absence of task instructions and training? We recorded EEG from macaque monkeys and humans while they passively listened to isochronous equitone sequences. Individual- and trial-level analyses showed that macaque monkeys' and humans' delta-band neural oscillations encoded and tracked the timing of auditory events. Further, mu- (8-15 Hz) and beta-band (12-20 Hz) oscillations revealed the superimposition of varied accentuation patterns on a subset of trials. These observations suggest convergence in the encoding and dynamic attending of temporal regularities in the acoustic environment, bridging a gap in the phylogenesis of rhythm cognition.

Sensory gating functions of the auditory thalamus: Adaptation and modulations through noise-exposure and high-frequency stimulation in rats.

The medial geniculate body (MGB) of the thalamus is an obligatory relay for auditory processing. A breakdown of adaptive filtering and sensory gating at this level may lead to multiple auditory dysfunctions, while high-frequency stimulation (HFS) of the MGB might mitigate aberrant sensory gating. To further investigate the sensory gating functions of the MGB, this study (i) recorded electrophysiological evoked potentials in response to continuous auditory stimulation, and (ii) assessed the effect of MGB HFS on these responses in noise-exposed and control animals. Pure-tone sequences were presented to assess differential sensory gating functions associated with stimulus pitch, grouping (pairing), and temporal regularity. Evoked potentials were recorded from the MGB and acquired before and after HFS (100 Hz). All animals (unexposed and noise-exposed, pre- and post-HFS) showed gating for pitch and grouping. Unexposed animals also showed gating for temporal regularity not found in noise-exposed animals. Moreover, only noise-exposed animals showed restoration comparable to the typical EP amplitude suppression following MGB HFS. The current findings confirm adaptive thalamic sensory gating based on different sound characteristics and provide evidence that temporal regularity affects MGB auditory signaling.

About time: Ageing influences neural markers of temporal predictability.

Timing abilities help organizing the temporal structure of events but are known to change systematically with age. Yet, how the neuronal signature of temporal predictability changes across the age span remains unclear. Younger (n = 21; 23.1 years) and older adults (n = 21; 68.5 years) performed an auditory oddball task, consisting of isochronous and random sound sequences. Results confirm an altered P50 response in the older compared to younger participants. P50 amplitudes differed between the isochronous and random temporal structures in younger, and for P200 in the older group. These results suggest less efficient sensory gating in older adults in both isochronous and random auditory sequences. N100 amplitudes were more negative for deviant tones. P300 amplitudes were parietally enhanced in younger, but not in older adults. In younger participants, the P50 results confirm that this component marks temporal predictability, indicating sensitive gating of temporally regular sound sequences.

Auditory thalamus dysfunction and pathophysiology in tinnitus: a predictive network hypothesis.

Tinnitus is the perception of a 'ringing' sound without an acoustic source. It is generally accepted that tinnitus develops after peripheral hearing loss and is associated with altered auditory processing. The thalamus is a crucial relay in the underlying pathways that actively shapes processing of auditory signals before the respective information reaches the cerebral cortex. Here, we review animal and human evidence to define thalamic function in tinnitus. Overall increased spontaneous firing patterns and altered coherence between the thalamic medial geniculate body (MGB) and auditory cortices is observed in animal models of tinnitus. It is likely that the functional connectivity between the MGB and primary and secondary auditory cortices is reduced in humans. Conversely, there are indications for increased connectivity between the MGB and several areas in the cingulate cortex and posterior cerebellar regions, as well as variability in connectivity between the MGB and frontal areas regarding laterality and orientation in the inferior, medial and superior frontal gyrus. We suggest that these changes affect adaptive sensory gating of temporal and spectral sound features along the auditory pathway, reflecting dysfunction in an extensive thalamo-cortical network implicated in predictive temporal adaptation to the auditory environment. Modulation of temporal characteristics of input signals might hence factor into a thalamo-cortical dysrhythmia profile of tinnitus, but could ultimately also establish new directions for treatment options for persons with tinnitus.

When temporal prediction errs: ERP responses to delayed action-feedback onset.

Sensory suppression effects observed in electroencephalography (EEG) index successful predictions of the type and timing of self-generated sensory feedback. However, it is unclear how precise the timing prediction of sensory feedback is, and how temporal delays between an action and its sensory feedback affect perception. The current study investigated how prediction errors induced by delaying tone onset times affect the processing of sensory feedback in audition. Participants listened to self-generated (via button press) or externally generated tones. Self-generated tones were presented either without or with various delays (50, 100, or 250 ms; in 30% of trials). Comparing listening to externally generated and self-generated tones resulted in action-related P50 amplitude suppression to tones presented immediately or 100 ms after the button press. Subsequent ERP responses became more sensitive to the type of delay. Whereas the comparison of actual and predicted sensory feedback (N1) tolerated temporal uncertainty up to 100 ms, P2 suppression was modulated by delay in a graded manner: suppression decreased with an increase in sensory feedback delay. Self-generated tones occurring 250 ms after the button press additionally elicited an enhanced N2 response. These findings suggest functionally dissociable processes within the forward model that are affected by the timing of sensory feedback to self-action: relative tolerance of temporal delay in the P50 and N1, confirming previous results, but increased sensitivity in the P2. Further, they indicate that temporal prediction errors are treated differently by the auditory system: only delays that occurred after a temporal integration window (∼100 ms) impact the conscious detection of altered sensory feedback.

Striatal contributions to sensory timing: Voxel-based lesion mapping of electrophysiological markers.

To achieve precise timing, the brain needs to establish a representation of the temporal structure of sensory input and use this information to generate timely responses. These operations engage the basal ganglia. Current research in this direction is limited by reliance on animal models, motor and/or offline tasks, small sample sizes, the low temporal resolution of functional magnetic resonance imaging, and the study of progressive neurodegeneration. Here, we combine the excellent temporal resolution of electrophysiological potentials with the high spatial resolution of structural neuroimaging to investigate basal ganglia contributions to sensory timing. Chronic-stage lesion patients and healthy controls listened to pure-tone sequences differing exclusively in temporal regularity. Event-related potentials (ERPs) indicate a selective indifference against this manipulation in patients, attributable to the striatal part of the basal ganglia on the basis of a lesion-mapping approach. These findings provide evidence for a crucial contribution of the basal ganglia to basic sensory functioning.

Effects of musically cued gait training in Parkinson's disease: beyond a motor benefit.

Auditory stimulation via rhythmic cues can be used successfully in the rehabilitation of motor function in patients with motor disorders. A prototypical example is provided by dysfunctional gait in patients with idiopathic Parkinson's disease (PD). Coupling steps to external rhythmic cues (the beat of music or the sounds of a metronome) leads to long-term motor improvements, such as increased walking speed and greater stride length. These effects are likely to be underpinned by compensatory brain mechanisms involving cerebellar-thalamocortical networks. Because these areas are also involved in perceptual and motor timing, parallel improvement in timing tasks is expected in PD beyond purely motor benefits. In keeping with this idea, we report here recent behavioral data showing beneficial effects of musically cued gait training (MCGT) on gait performance (i.e., increased stride length and speed), perceptual timing (e.g., discriminating stimulus durations), and sensorimotor timing abilities (i.e., in paced tapping tasks) in PD patients. Particular attention is paid to individual differences in timing abilities in PD, thus paving the ground for an individualized MCGT-based therapy.

Temporal dynamics of contingency extraction from tonal and verbal auditory sequences.

Consecutive sound events are often to some degree predictive of each other. Here we investigated the brain's capacity to detect contingencies between consecutive sounds by means of electroencephalography (EEG) during passive listening. Contingencies were embedded either within tonal or verbal stimuli. Contingency extraction was measured indirectly via the elicitation of the mismatch negativity (MMN) component of the event-related potential (ERP) by contingency violations. MMN results indicate that structurally identical forms of predictability can be extracted from both tonal and verbal stimuli. We also found similar generators to underlie the processing of contingency violations across stimulus types, as well as similar performance in an active-listening follow-up test. However, the process of passive contingency extraction was considerably slower (twice as many rule exemplars were needed) for verbal than for tonal stimuli These results suggest caution in transferring findings on complex predictive regularity processing obtained with tonal stimuli directly to the speech domain.

Cerebellum, temporal predictability and the updating of a mental model.

We live in a dynamic and changing environment, which necessitates that we adapt to and efficiently respond to changes of stimulus form ('what') and stimulus occurrence ('when'). Consequently, behaviour is optimal when we can anticipate both the 'what' and 'when' dimensions of a stimulus. For example, to perceive a temporally expected stimulus, a listener needs to establish a fairly precise internal representation of its external temporal structure, a function ascribed to classical sensorimotor areas such as the cerebellum. Here we investigated how patients with cerebellar lesions and healthy matched controls exploit temporal regularity during auditory deviance processing. We expected modulations of the N2b and P3b components of the event-related potential in response to deviant tones, and also a stronger P3b response when deviant tones are embedded in temporally regular compared to irregular tone sequences. We further tested to what degree structural damage to the cerebellar temporal processing system affects the N2b and P3b responses associated with voluntary attention to change detection and the predictive adaptation of a mental model of the environment, respectively. Results revealed that healthy controls and cerebellar patients display an increased N2b response to deviant tones independent of temporal context. However, while healthy controls showed the expected enhanced P3b response to deviant tones in temporally regular sequences, the P3b response in cerebellar patients was significantly smaller in these sequences. The current data provide evidence that structural damage to the cerebellum affects the predictive adaptation to the temporal structure of events and the updating of a mental model of the environment under voluntary attention.

Dissociation of formal and temporal predictability in early auditory evoked potentials.

Perceived regularity among events in the environment allows predictions regarding the "when" and the "what" dimensions of future events. In this context, one crucial question concerns the impact and the potentially optimizing effect, of regular temporal structure on the processing of "what", or formal, information. The current study addresses this issue by investigating whether temporal and formal structure interact during early stages of sensory processing, and by relating the respective findings to the concept of a predictive bias in brain function. Analyses were performed on two components of the auditory event-related-potential of the electroencephalogram, namely the P50 and the N100. Oddball sequences consisting of frequent standard and infrequent deviant sinusoidal tones were presented with either regular or irregular temporal structure in pre-attentive and attentive experimental settings (Schwartze, Rothermich, Schmidt-Kassow, & Kotz, 2011). Temporal regularity effects on pre-attentive and attentive processing of deviance. Biological Psychology, 87, 146-151). The results confirm that the P50 and the N100 amplitudes reliably encode formal and temporal predictability. Similar patterns of results obtained with pre-attentive and attentive task instructions, as well as the absence of a significant interaction of formal and temporal structure suggest that the P50 response may be interpreted as an automatic marker of predictability, whereas the N100 may represent a more complex marker, in which formal and temporal structure start interacting as a function of attention.

Temporal regularity effects on pre-attentive and attentive processing of deviance.

Temporal regularity allows predicting the temporal locus of future information thereby potentially facilitating cognitive processing. We applied event-related brain potentials (ERPs) to investigate how temporal regularity impacts pre-attentive and attentive processing of deviance in the auditory modality. Participants listened to sequences of sinusoidal tones differing exclusively in pitch. The inter-stimulus interval (ISI) in these sequences was manipulated to convey either isochronous or random temporal structure. In the pre-attentive session, deviance processing was unaffected by the regularity manipulation as evidenced in three event-related-potentials (ERPs): mismatch negativity (MMN), P3a, and reorienting negativity (RON). In the attentive session, the P3b was smaller for deviant tones embedded in irregular temporal structure, while the N2b component remained unaffected. These findings confirm that temporal regularity can reinforce cognitive mechanisms associated with the attentive processing of deviance. Furthermore, they provide evidence for the dynamic allocation of attention in time and dissociable pre-attentive and attention-dependent temporal processing mechanisms.

Non-motor basal ganglia functions: a review and proposal for a model of sensory predictability in auditory language perception.

While the primary function of the basal ganglia (BG) is linked to motor behaviour, several investigations of non-motor behaviour allocate cognitive and language-specific functions to the BG. What may such seemingly discrepant functions have in common? Some neurophysiologic theories of motor behaviour assign temporal sequencing, others the sequencing of general cognitive patterns to the BG. Turning to auditory language perception and syntax in particular, one may consider syntactic processing as a hierarchical sequencing phenomenon. Furthermore, previous data have shown that if events are predictable, the processing of successively following events in a sequence is facilitated. We propose that sequencing is closely linked to the perception of predictable cues (regular beats, meter, temporal chunks etc.). If this is the case, syntactic processing should rely on the extraction of predictable cues in auditory language perception. Consequently, dysfunctional extraction of such cues in BG patients should then lead to secondary deficits in syntactic processing as evidenced in recent behavioural and electrophysiological evidence (ERP). The fact that such "secondary syntactic deficits" can be compensated by external and speech inherent predictable cues permits two conclusions: (i) syntactic deficits in BG patients are epiphenomenal, and (ii) sequencing dysfunctions of the pre-supplementary motor area (SMA)-BG circuit may be compensated by increased influence of the cerebellar-thalamic-pre-SMA pathway. In the current review we elaborate on this possibility drawing comparisons to similar proposals in motor and language production.