Biology subjects

Pittman-Polletta, B. R.

Publications and source records attributed to Pittman-Polletta, B. R..

7 recordsLinked to original sources

bioRxiv2025

Auditory-motor synchronization determines the use of predictions in music perception

When listening to music, our brain constantly generates predictions about the timing and pitch of upcoming sounds based on the structure of the music. Individual differences in the ability to make such rhythmic and melodic predictions shape music perception. Previous studies show that during rhythmic auditory-motor synchronization tasks, better performance is related to stronger motor system engagement. However, whether individual differences in auditory-motor interactions influence higher-level rhythmic predictions is unknown. Here, we used electroencephalography during a naturalistic music listening task to assess the neural tracking of rhythmic and melodic predictions generated from (short-term) local contextual information and (long-term) experience using the Information Dynamics of Music model. We combined a multivariate temporal response function approach with two behavioral measures of auditory-motor synchronization (whispering and finger tapping). We found that stronger auditory-motor synchronization predicted stronger neural tracking of lower-level temporal aspects of the music signal, i.e. acoustic envelope and note onset. Across participants, higher-level (short- and long-term) predictions were also neurally tracked, with neural tracking stronger for rhythmic than melodic predictions. Importantly, our evidence suggests individual differences in the weighting of musical predictions. Individuals with stronger auditory-motor synchronization showed stronger neural tracking of rhythmic compared to melodic predictions, and this effect was especially pronounced for short-term predictions. Our findings demonstrate that the motor system is critically involved at several processing levels even in purely perceptual music tasks, and pave the way for understanding individual differences in the weighting of rhythmic and melodic predictions during music listening. Significance statementOur ability to make musical predictions affects our perception of music. Understanding individual differences in predictive processing may allow for differential diagnostics and interventions in clinical disorders such as rhythm disorders or hearing impairment. In an electrophysiological study, we found evidence that the motor system is implicated in predictive processes during perception of music. Specifically, we find advanced neural processing of acoustic temporal features and stronger weighting of short- and long-term rhythmic musical predictions in individuals who recruit the motor system more strongly. Likely, in individuals with high compared to low auditory-motor synchronization strength, the motor system facilitates temporal processing at different levels: at the level of acoustic temporal structure processing, and at higher-level processing of rhythmic musical predictions.

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bioRxiv2020

Differential contributions of synaptic and intrinsic inhibitory currents to parsing via flexible phase-locking in neural oscillators

Current hypotheses suggest that speech segmentation - the initial division and grouping of the speech stream into candidate phrases, syllables, and phonemes for further linguistic processing - is executed by a hierarchy of oscillators in auditory cortex. Theta (~3-12 Hz) rhythms play a key role by phase-locking to recurring acoustic features marking syllable boundaries. Reliable synchronization to quasi-rhythmic inputs, whose variable frequency can dip below cortical theta frequencies (down to ~1 Hz), requires "flexible" theta oscillators whose underlying neuronal mechanisms remain unknown. Using biophysical computational models, we found that the flexibility of phase-locking in neural oscillators depended on the types of hyperpolarizing currents that paced them. Simulated cortical theta oscillators flexibly phase-locked to slow inputs when these inputs caused both (i) spiking and (ii) the subsequent buildup of outward current sufficient to delay further spiking until the next input. The greatest flexibility in phase-locking arose from a synergistic interaction between intrinsic currents that was not replicated by synaptic currents at similar timescales. Flexibility in phase-locking enabled improved entrainment to speech input, optimal at mid-vocalic channels, which in turn supported syllabic-timescale segmentation through identification of vocalic nuclei. Our results suggest that synaptic and intrinsic inhibition contribute to frequency-restricted and -flexible phase-locking in neural oscillators, respectively. Their differential deployment may enable neural oscillators to play diverse roles, from reliable internal clocking to adaptive segmentation of quasi-regular sensory inputs like speech. Author summaryOscillatory activity in auditory cortex is believed to play an important role in auditory and speech processing. One suggested function of these rhythms is to divide the speech stream into candidate phonemes, syllables, words, and phrases, to be matched with learned linguistic templates. This requires brain rhythms to flexibly synchronize with regular acoustic features of the speech stream. How neuronal circuits implement this task remains unknown. In this study, we explored the contribution of inhibitory currents to flexible phase-locking in neuronal theta oscillators, believed to perform initial syllabic segmentation. We found that a combination of specific intrinsic inhibitory currents at multiple timescales, present in a large class of cortical neurons, enabled exceptionally flexible phase-locking, which could be used to precisely segment speech by identifying vowels at mid-syllable. This suggests that the cells exhibiting these currents are a key component in the brains auditory and speech processing architecture.

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bioRxiv2019

Flexible reset and entrainment of delta oscillations in primate primary auditory cortex: modeling and experiment

Salient auditory stimuli typically exhibit rhythmic temporal patterns. A growing body of evidence suggests that, in primary auditory cortex (A1), attention is associated with entrainment of delta rhythms (1 - 4 Hz) by these auditory stimuli. It is thought that this entrainment involves phase reset of ongoing spontaneous oscillations in A1 by thalamus matrix afferents, but precise mechanisms are unknown. Furthermore, naturalistic stimuli can vary widely in terms of their rhythmicity: some cycles can be longer than others and frequency can drift over time. It is not clear how the auditory system accommodates this natural variability. We show that in rhesus macaque monkey A1 in vivo, bottom-up gamma (40 Hz) click trains influence ongoing spontaneous delta rhythms by inducing an initial delta-timescale transient response, followed by entrainment to gamma and suppression of delta. We then construct a computational model to reproduce this effect, showing that transient thalamus matrix activation can reset A1 delta oscillations by directly activating deep (layer 5) IB cells, promoting bursting, and beginning a new delta cycle. In contrast, long duration gamma-rhythmic input stimuli induce a steady-state containing entrainment of superficial RS and FS cells at gamma, and suppression of delta oscillations. This suppression is achieved in the model by two complementary pathways. First, long-duration thalamus matrix input causes IB cells to switch from bursting to sparse firing, which disrupts the IB bursts associated with delta. Second, thalamus core input activates deep FS cells (by way of layer 4), which fire at gamma frequency and actively inhibit the delta oscillator. Together, these two fundamental operations of reset and suppression can respectively advance and delay the phase of the delta oscillator, allowing it to follow rhythms exhibiting the type of variability found in the natural environment. We discuss these findings in relation to functional implications for speech processing.\n\nAuthor summaryNeurons organize their firing into synchronous, rhythmic patterns. These neural oscillations have been shown to entrain to rhythmic stimuli in the external world, such as patterns of speech or patterns of movement. By entraining to a particular input stimulus, these oscillations are thought to help us attend to that stimulus and to exclude others. To understand how this synchronization emerges, we constructed a physiologically detailed mathematical model of the primary auditory cortex. By fitting this model to a variety of experimental data, we suggest fundamental mechanisms by which neurons of the auditory cortex can synchronize their activity to rhythmic external stimuli. This result will be useful for understanding the mechanism and limitations of oscillatory entrainment, which are thought to underlie the processing of naturalistic auditory inputs like speech or music. Furthermore, this model, though simplified, was shown to generalize and reproduce a wide range of experimental results, and can thus be used as a starting point for building more complex models of auditory cortex.

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bioRxiv2019

A biophysical model of striatal microcircuits suggests theta-rhythmically interleaved gamma and beta oscillations mediate periodicity in motor control

Striatal oscillatory activity is associated with movement, reward, and decision-making, and observed in several interacting frequency bands. Local field potential recordings in rodent striatum show dopamine- and reward-dependent transitions between two states: a "spontaneous" state involving {beta} (~15-30 Hz) and low{gamma} (~40-60 Hz), and a state involving{theta} (~4-8 Hz) and high{gamma} (~60-100 Hz) in response to dopaminergic agonism and reward. The mechanisms underlying these rhythmic dynamics, their interactions, and their functional consequences are not well understood. In this paper, we propose a biophysical model of striatal microcircuits that comprehensively describes the generation and interaction of these rhythms, as well as their modulation by dopamine. Building on previous modeling and experimental work suggesting that striatal projection neurons (SPNs) are capable of generating {beta} oscillations, we show that networks of striatal fast-spiking interneurons (FSIs) are capable of generating{delta} /{theta} (ie, 2 to 6 Hz) and{gamma} rhythms. Under simulated low dopaminergic tone our model FSI network produces low{gamma} band oscillations, while under high dopaminergic tone the FSI network produces high{gamma} band activity nested within a{delta} /{theta} oscillation. SPN networks produce {beta} rhythms in both conditions, but under high dopaminergic tone, this {beta} oscillation is interrupted by{delta} /{theta}-periodic bursts of{gamma} -frequency FSI inhibition. Thus, in the high dopamine state, packets of FSI{gamma} and SPN {beta} alternate at a{delta} /{theta} timescale. In addition to a mechanistic explanation for previously observed rhythmic interactions and transitions, our model suggests a hypothesis as to how the relationship between dopamine and rhythmicity impacts motor function. We hypothesize that high dopamine-induced periodic FSI{gamma} -rhythmic inhibition enables switching between {beta}-rhythmic SPN cell assemblies representing the currently active motor program, and thus that dopamine facilitates movement in part by allowing for rapid, periodic shifts in motor program execution. Author summaryStriatal oscillatory activity is associated with movement, reward, and decision-making, and observed in several interacting frequency bands. The mechanisms underlying these rhythmic dynamics, their interactions, and their functional consequences are not well understood. In this paper, we propose a biophysical model of striatal microcircuits that comprehensively describes the generation and interaction of striatal rhythms, as well as their modulation by dopamine. Our model suggests a hypothesis as to how the relationship between dopamine and rhythmicity impacts the function of the motor system, enabling rapid, periodic shifts in motor program execution.

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bioRxiv2018

Biased competition in the absence of input bias: predictions from corticostriatal computation

Classical accounts of biased competition (BC) require an input bias to resolve the competition between neuronal ensembles driving downstream processing. However, flexible and reliable selection of behaviorally-relevant ensembles can occur with unbiased stimulation: striatal D1 and D2 spiny projecting neurons (SPNs) receive balanced cortical input, yet their activity determines the choice between GO and NO-GO pathways in the basal ganglia. We present a corticostriatal model identifying three mechanisms that rely on physiological asymmetries to effect rate- and time-coded BC in the presence of balanced inputs. First, tonic input strength determines which SPN phenotype exhibit higher mean firing rate (FR). Second, low strength oscillatory inputs induce higher FR in D2 SPNs but higher coherence between D1 SPNs. Third, high strength inputs oscillating at distinct frequencies preferentially activate D1 or D2 SPN populations. Of these mechanisms, the latter accommodates observed rhythmic activity supporting rule-based decision making in prefrontal cortex.

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bioRxiv2017

Modeling the schizophrenias: subunit-specific NMDAR antagonism dissociates oscillatory signatures of frontal hypofunction and hippocampal hyperfunction

NMDAR antagonism alters mesolimbic, hippocampal, and cortical function, acutely reproducing the positive, cognitive, and negative symptoms of schizophrenia. These physiological and behavioral effects may depend differentially on NMDAR subtype-and region-specific effects. The dramatic electrophysiological signatures of NMDAR blockade in rodents include potentiated high frequency oscillations (HFOs, ~140 Hz), likely generated in mesolimbic structures, and increased HFO phase-amplitude coupling (PAC), a phenomenon related to goal-directed behavior and dopaminergic tone. This study examined the impact of subtype-specific NMDAR antagonism on HFOs and PAC. We found that positive-symptom-associated NR2A-preferring antagonism (NVP-AAM077), but not NR2B-specific antagonism (Ro25-6985) or saline control, replicated increases in HFO power seen with nonspecific antagonism (MK-801). However, PAC following NR2A-preferring antagonism was distinct from all other conditions. While{theta} -HFO PAC was prominent or potentiated in other conditions, NVP-AAM077 increased{delta} -HFO PAC and decreased{theta} -HFO PAC. Furthermore, active wake epochs exhibiting narrowband frontal{delta} oscillations, and not broadband sleep-associated{delta} , selectively exhibited{delta} -HFO coupling, while paradoxical sleep epochs having a high CA1{theta} to frontal{delta} ratio selectively exhibited{theta} -HFO coupling. Our results suggest: (1) NR2A-preferring antagonism induces oscillopathies re[fl]ecting frontal hyperfunction and hippocampal hypofunction; and (2) HFO PAC indexes cortical vs. hippocampal control of mesolimbic circuits.

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bioRxiv2017

Striatal cholinergic receptor activation causes a rapid, selective, & state-dependent rise in corticostriatal β activity.

Cortico-basal ganglia-thalamic (CBT) {beta} oscillations (15-30 Hz) are elevated in Parkinsons disease and correlated with movement disability. To date, no experimental paradigm outside of loss of dopamine has been able to specifically elevate {beta} oscillations in the CBT loop. Here, we show that activation of striatal cholinergic receptors selectively increased {beta} oscillations in mouse striatum and motor cortex. In individuals showing simultaneous {beta} increases in both striatum and M1, {beta} partial directed coherence (PDC) increased from striatum to M1 (but not in the reverse direction). In individuals that did not show simultaneous {beta} increases, {beta} PDC increased from M1 to striatum (but not in the reverse direction), and M1 was characterized by persistent {beta}-HFO phase-amplitude coupling. Finally, the direction of {beta} PDC distinguished between {beta} subbands. This suggests: (1) striatal cholinergic tone exerts state-dependent and frequency-selective control over CBT {beta} power and coordination; (2) ongoing rhythmic dynamics can determine whether elevated {beta} oscillations are expressed in striatum and M1; (3) altered striatal cholinergic tone differentially modulates distinct {beta} subbands.

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